Variation in Gut Microbiota Composition is Associated with Sleep Quality and Cognitive Performance in Older Adults with Insomnia

References

• Shochat T, Ancoli-Israel S. Chapter 153 - insomnia in older adults. In: Kryger M, Roth T, Dement WC, editors. Principles and Practice of Sleep Medicine. 6th ed. Elsevier; 2017:1503–1509.e4.
   Google Scholar
• Haimov I, Hanuka E, Horowitz Y. Chronic insomnia and cognitive functioning among older adults. Behav Sleep Med. 2008;6(1):32–54. doi:10.1080/15402000701796080
   PubMed Web of Science ®Google Scholar
• Riemann D, Nissen C, Palagini L, Otte A, Perlis ML, Spiegelhalder K. The neurobiology, investigation, and treatment of chronic insomnia. Lancet Neurol. 2015;14(5):547–558. doi:10.1016/S1474-4422(15)00021-6
   PubMed Web of Science ®Google Scholar
• Karlson CW, Gallagher MW, Olson CA, Hamilton NA. Insomnia symptoms and well-being: longitudinal follow-up. Health Psychol. 2013;32(3):311–319. doi:10.1037/a0028186
   PubMed Web of Science ®Google Scholar
• Suh S, Yang HC, Kim N, et al. Chronotype differences in health behaviors and health-related quality of life: a population-based study among aged and older adults. Behav Sleep Med. 2017;15(5):361–376. doi:10.1080/15402002.2016.1141768
   PubMed Web of Science ®Google Scholar
• Zaslavsky O, LaCroix AZ, Hale L, Tindle H, Shochat T. Longitudinal changes in insomnia status and incidence of physical, emotional, or mixed impairment in postmenopausal women participating in the Women’s Health Initiative (WHI) study. Sleep Med. 2015;16(3):364–371. doi:10.1016/j.sleep.2014.11.008
   PubMed Web of Science ®Google Scholar
• Bassuk SS, Wypij D, Berkman LF. Cognitive impairment and mortality in the community-dwelling elderly. Am J Epidemiol. 2000;151(7):676–688. doi:10.1093/oxfordjournals.aje.a010262
   PubMed Web of Science ®Google Scholar
• Ostbye T, Steenhuis R, Wolfson C, Walton R, Hill G. Predictors of five-year mortality in older Canadians: the Canadian study of health and aging. J Am Geriatr Soc. 1999;47(10):1249–1254. doi:10.1111/j.1532-5415.1999.tb05207.x
   PubMed Web of Science ®Google Scholar
• Diekelmann S, Born J. The memory function of sleep. Nat Rev Neurosci. 2010;11(2):114–126. doi:10.1038/nrn2762
   PubMed Web of Science ®Google Scholar
• Walker MP, Stickgold R. Sleep-dependent learning and memory consolidation. Neuron. 2004;44(1):121–133. doi:10.1016/j.neuron.2004.08.031
   PubMed Web of Science ®Google Scholar
• Cerasuolo M, Conte F, Giganti F, Ficca G. Sleep changes following intensive cognitive activity. Sleep Med. 2020;66:148–158. doi:10.1016/j.sleep.2019.08.016
   PubMed Web of Science ®Google Scholar
• Fogel SM, Smith CT. Learning-dependent changes in sleep spindles and stage 2 sleep. J Sleep Res. 2006;15(3):250–255. doi:10.1111/j.1365-2869.2006.00522.x
   PubMed Web of Science ®Google Scholar
• Huber R, Felice Ghilardi M, Massimini M, Tononi G. Local sleep and learning. Nature. 2004;430(6995):78–81. doi:10.1038/nature02663
   PubMed Web of Science ®Google Scholar
• Peters KR, Smith V, Smith CT. Changes in sleep architecture following motor learning depend on initial skill level. J Cogn Neurosci. 2007;19(5):817–829. doi:10.1162/jocn.2007.19.5.817
   PubMed Web of Science ®Google Scholar
• Peters KR, Ray L, Smith V, Smith C. Changes in the density of stage 2 sleep spindles following motor learning in young and older adults. J Sleep Res. 2008;17(1):23–33. doi:10.1111/j.1365-2869.2008.00634.x
   PubMed Web of Science ®Google Scholar
• Schabus M, Gruber G, Parapatics S, et al. Sleep spindles and their significance for declarative memory consolidation. Sleep. 2004;27(8):1479–1485. doi:10.1093/sleep/27.7.1479
   PubMed Web of Science ®Google Scholar
• Smith CT, Nixon MR, Nader RS. Posttraining increases in REM sleep intensity implicate REM sleep in memory processing and provide a biological marker of learning potential. Learn Mem. 2004;11(6):714–719. doi:10.1101/lm.74904
   PubMed Web of Science ®Google Scholar
• Arzilli C, Cerasuolo M, Conte F, et al. The effect of cognitive activity on sleep maintenance in a subsequent daytime nap. Behav Sleep Med. 2019;17(5):552–560. doi:10.1080/15402002.2018.1425870
   PubMed Web of Science ®Google Scholar
• Cerasuolo M, Conte F, Cellini N, et al. The effect of complex cognitive training on subsequent night sleep. J Sleep Res. 2020;29(6):e12929. doi:10.1111/jsr.12929
   PubMed Web of Science ®Google Scholar
• de Koninck J, Lorrain D, Christ G, Proulx G, Coulombe D. Intensive language learning and increases in rapid eye movement sleep: evidence of a performance factor. Int J Psychophysiol. 1989;8(1):43–47. doi:10.1016/0167-8760(89)90018-4
   PubMed Web of Science ®Google Scholar
• Smith C, Lapp L. Increases in number of REMS and REM density in humans following an intensive learning period. Sleep. 1991;14(4):325–330. doi:10.1093/sleep/14.4.325
   PubMed Web of Science ®Google Scholar
• Fogel SM, Smith CT, Cote KA. Dissociable learning-dependent changes in REM and non-REM sleep in declarative and procedural memory systems. Behav Brain Res. 2007;180(1):48–61. doi:10.1016/j.bbr.2007.02.037
   PubMed Web of Science ®Google Scholar
• Naylor E, Penev PD, Orbeta L, et al. Daily social and physical activity increases slow-wave sleep and daytime neuropsychological performance in the elderly. Sleep. 2000;23(1):1–9. doi:10.1093/sleep/23.1.1f
   Web of Science ®Google Scholar
• Conte F, Carobbi G, Errico B, Ficca G. The effects of pre-sleep learning on sleep continuity, stability, and organization in elderly individuals. Front Neurol. 2012;3. doi:10.3389/fneur.2012.00109
   PubMedGoogle Scholar
• Haimov I, Shatil E. Cognitive training improves sleep quality and cognitive function among older adults with insomnia. PLoS One. 2013;8(4):e61390. doi:10.1371/journal.pone.0061390
   PubMed Web of Science ®Google Scholar
• Keramtinejad M, Azadi A, Taghinejad H, Khorshidi A. The effectiveness of cognitive training on improving cognitive function and sleep quality in community-dwelling elderly in Iran. Sleep Sci. 2019;12(2):88–93. doi:10.5935/1984-0063.20190065
   PubMed Web of Science ®Google Scholar
• Cryan JF, O’Riordan KJ, Cowan CSM, et al. The microbiota-gut-brain axis. Physiol Rev. 2019;99(4):1877–2013. doi:10.1152/physrev.00018.2018
   PubMed Web of Science ®Google Scholar
• Foster JA, Rinaman L, Cryan JF. Stress & the gut-brain axis: regulation by the microbiome. Neurobiol Stress. 2017;7:124–136. doi:10.1016/j.ynstr.2017.03.001
   PubMed Web of Science ®Google Scholar
• Forsythe P, Sudo N, Dinan T, Taylor VH, Bienenstock J. Mood and gut feelings. Brain Behav Immun. 2010;24(1):9–16. doi:10.1016/j.bbi.2009.05.058
   PubMed Web of Science ®Google Scholar
• Rhee SH, Pothoulakis C, Mayer EA. Principles and clinical implications of the brain-gut-enteric microbiota axis. Nat Rev Gastroenterol Hepatol. 2009;6(5):306–314. doi:10.1038/nrgastro.2009.35
   PubMed Web of Science ®Google Scholar
• Dinan TG, Cryan JF. The microbiome-gut-brain axis in health and disease. Gastroenterol Clin North Am. 2017;46(1):77–89. doi:10.1016/j.gtc.2016.09.007
   PubMed Web of Science ®Google Scholar
• Foster JA, McVey Neufeld KA. Gut-brain axis: how the microbiome influences anxiety and depression. Trends Neurosci. 2013;36(5):305–312. doi:10.1016/j.tins.2013.01.005
   PubMed Web of Science ®Google Scholar
• Jiang H, Ling Z, Zhang Y, et al. Altered fecal microbiota composition in patients with major depressive disorder. Brain Behav Immun. 2015;48:186–194. doi:10.1016/j.bbi.2015.03.016
   PubMed Web of Science ®Google Scholar
• Li Y, Hao Y, Fan F, Zhang B. The role of microbiome in insomnia, circadian disturbance and depression. Front Psychiatry. 2018;9:669. doi:10.3389/fpsyt.2018.00669
   PubMed Web of Science ®Google Scholar
• Hufeldt MR, Nielsen DS, Vogensen FK, Midtvedt T, Hansen AK. Variation in the gut microbiota of laboratory mice is related to both genetic and environmental factors. Comp Med. 2010;60(5):336–347.
   PubMed Web of Science ®Google Scholar
• Turnbaugh PJ, Ridaura VK, Faith JJ, Rey FE, Knight R, Gordon JI. The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice. Sci Transl Med. 2009;1(6):6ra14–6ra14. doi:10.1126/scitranslmed.3000322
   PubMed Web of Science ®Google Scholar
• Cho I, Yamanishi S, Cox L, et al. Antibiotics in early life alter the murine colonic microbiome and adiposity. Nature. 2012;488(7413):621–626. doi:10.1038/nature11400
   PubMed Web of Science ®Google Scholar
• Yatsunenko T, Rey FE, Manary MJ, 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
• Appanna VD. What if the workings of the microbiome are fully uncovered? – a revolution in human health, wellness and beyond. In: Appanna VD, editor. Human Microbes - The Power Within: Health, Healing and Beyond. Springer; 2018:123–159. doi:10.1007/978-981-10-7684-8_4
   Google Scholar
• An R, Wilms E, Masclee AAM, Smidt H, Zoetendal EG, Jonkers D. Age-dependent changes in GI physiology and microbiota: time to reconsider? Gut. 2018;67(12):2213–2222. doi:10.1136/gutjnl-2017-315542
   PubMed Web of Science ®Google Scholar
• Mariat D, Firmesse O, Levenez F, et al. The Firmicutes/Bacteroidetes ratio of the human microbiota changes with age. BMC Microbiol. 2009;9:123. doi:10.1186/1471-2180-9-123
   PubMed Web of Science ®Google Scholar
• Abenavoli L, Scarpellini E, Colica C, et al. Gut microbiota and obesity: a role for probiotics. Nutrients. 2019;11(11):E2690. doi:10.3390/nu11112690
   PubMed Web of Science ®Google Scholar
• Shen ZH, Zhu CX, Quan YS, et al. Relationship between intestinal microbiota and ulcerative colitis: mechanisms and clinical application of probiotics and fecal microbiota transplantation. World J Gastroenterol. 2018;24(1):5–14. doi:10.3748/wjg.v24.i1.5
   PubMed Web of Science ®Google Scholar
• Liu B, Lin W, Chen S, et al. Gut microbiota as an objective measurement for auxiliary diagnosis of insomnia disorder. Front Microbiol. 2019;10:1770. doi:10.3389/fmicb.2019.01770
   PubMed Web of Science ®Google Scholar
• Benedict C, Vogel H, Jonas W, et al. Gut microbiota and glucometabolic alterations in response to recurrent partial sleep deprivation in normal-weight young individuals. Mol Metab. 2016;5(12):1175–1186. doi:10.1016/j.molmet.2016.10.003
   PubMed Web of Science ®Google Scholar
• Zhang SL, Bai L, Goel N, et al. Human and rat gut microbiome composition is maintained following sleep restriction. Proc Natl Acad Sci USA. 2017;114(8):E1564–E1571. doi:10.1073/pnas.1620673114
   PubMed Web of Science ®Google Scholar
• Anderson JR, Carroll I, Azcarate-Peril MA, et al. A preliminary examination of gut microbiota, sleep, and cognitive flexibility in healthy older adults. Sleep Med. 2017;38:104–107. doi:10.1016/j.sleep.2017.07.018
   PubMed Web of Science ®Google Scholar
• Minter MR, Hinterleitner R, Meisel M, et al. Antibiotic-induced perturbations in microbial diversity during post-natal development alters amyloid pathology in an aged APPSWE/PS1ΔE9 murine model of Alzheimer’s disease. Sci Rep. 2017;7(1):10411. doi:10.1038/s41598-017-11047-w
   PubMed Web of Science ®Google Scholar
• Gareau MG, Wine E, Rodrigues DM, et al. Bacterial infection causes stress-induced memory dysfunction in mice. Gut. 2011;60(3):307–317. doi:10.1136/gut.2009.202515
   PubMed Web of Science ®Google Scholar
• Gareau MG. Cognitive function and the microbiome. Int Rev Neurobiol. 2016;131:227–246. doi:10.1016/bs.irn.2016.08.001
   PubMed Web of Science ®Google Scholar
• Meyer K, Lulla A, Debroy K, et al. Association of the gut microbiota with cognitive function in midlife. JAMA Netw Open. 2022;5(2):e2143941. doi:10.1001/jamanetworkopen.2021.43941
   PubMed Web of Science ®Google Scholar
• Kalmbach DA, Pillai V, Arnedt JT, Drake CL. DSM-5 insomnia and short sleep: comorbidity landscape and racial disparities. Sleep. 2016;39(12):2101–2111. doi:10.5665/sleep.6306
   PubMed Web of Science ®Google Scholar
• Lichstein KL, Durrence HH, Taylor DJ, Bush AJ, Riedel BW. Quantitative criteria for insomnia. Behav Res Ther. 2003;41(4):427–445. doi:10.1016/S0005-7967(02)00023-2
   PubMed Web of Science ®Google Scholar
• Buysse DJ, Ancoli-Israel S, Edinger JD, Lichstein KL, Morin CM. Recommendations for a standard research assessment of insomnia. Sleep. 2006;29(9):1155–1173. doi:10.1093/sleep/29.9.1155
   PubMed Web of Science ®Google Scholar
• Kukull WA, Larson EB, Teri L, Bowen J, McCormick W, Pfanschmidt ML. The mini-mental state examination score and the clinical diagnosis of dementia. J Clin Epidemiol. 1994;47(9):1061–1067. doi:10.1016/0895-4356(94)90122-8
   PubMed Web of Science ®Google Scholar
• Bastien CH, Vallières A, Morin CM. Validation of the insomnia severity index as an outcome measure for insomnia research. Sleep Med. 2001;2(4):297–307. doi:10.1016/s1389-9457(00)00065-4
   PubMed Web of Science ®Google Scholar
• Cho YW, Song ML, Morin CM. Validation of a Korean version of the insomnia severity index. J Clin Neurol. 2014;10(3):210–215. doi:10.3988/jcn.2014.10.3.210
   PubMed Web of Science ®Google Scholar
• Robbins TW, James M, Owen AM, Sahakian BJ, McInnes L, Rabbitt P. Cambridge Neuropsychological Test Automated Battery (CANTAB): a factor analytic study of a large sample of normal elderly volunteers. Dementia. 1994;5(5):266–281. doi:10.1159/000106735
   PubMedGoogle Scholar
• Lenehan ME, Summers MJ, Saunders NL, Summers JJ, Vickers JC. Does the Cambridge Automated Neuropsychological Test Battery (CANTAB) distinguish between cognitive domains in healthy older adults? Assessment. 2016;23(2):163–172. doi:10.1177/1073191115581474
   PubMed Web of Science ®Google Scholar
• Soares FC, de Oliveira TCG, de Macedo LDED, et al. CANTAB object recognition and language tests to detect aging cognitive decline: an exploratory comparative study. Clin Interv Aging. 2015;10:37–48. doi:10.2147/CIA.S68186
   PubMedGoogle Scholar
• Parada AE, Needham DM, Fuhrman JA. Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environ Microbiol. 2016;18(5):1403–1414. doi:10.1111/1462-2920.13023
   PubMed Web of Science ®Google Scholar
• Apprill A, McNally S, Parsons R, Weber L. Minor revision to V4 region SSU rRNA 806R gene primer greatly increases detection of SAR11 bacterioplankton. Aquat Microb Ecol. 2015;75(2):129–137. doi:10.3354/ame01753
   Web of Science ®Google Scholar
• Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP. DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13(7):581–583. doi:10.1038/nmeth.3869
   PubMed Web of Science ®Google Scholar
• Glöckner FO, Yilmaz P, Quast C, et al. 25 years of serving the community with ribosomal RNA gene reference databases and tools. J Biotechnol. 2017;261:169–176. doi:10.1016/j.jbiotec.2017.06.1198
   PubMed Web of Science ®Google Scholar
• Paulson JN, Stine OC, Bravo HC, Pop M. Differential abundance analysis for microbial marker-gene surveys. Nat Methods. 2013;10(12):1200–1202. doi:10.1038/nmeth.2658
   PubMed Web of Science ®Google Scholar
• Falony G, Joossens M, Vieira-Silva S, et al. Population-level analysis of gut microbiome variation. Science. 2016;352(6285):560–564. doi:10.1126/science.aad3503
   PubMed Web of Science ®Google Scholar
• Landry G, Best J, Liu-Ambrose T. Measuring sleep quality in older adults: a comparison using subjective and objective methods. Front Aging Neurosci. 2015;7. doi:10.3389/fnagi.2015.00166
   Google Scholar
• Haimov I, Breznitz N, Shiloh S. Sleep in healthy elderly: correlates of the discrepancy between self-report and recorded sleep. Proceedings of the 2nd Interim Congress of the World Federation of Sleep Research and Sleep Medicine Societies; 2005:145–147.
   Google Scholar
• Grosicki GJ, Riemann BL, Flatt AA, Valentino T, Lustgarten MS. Self-reported sleep quality is associated with gut microbiome composition in young, healthy individuals: a pilot study. Sleep Med. 2020;73:76–81. doi:10.1016/j.sleep.2020.04.013
   PubMed Web of Science ®Google Scholar
• Agrawal R, Ajami NJ, Malhotra S, et al. Habitual sleep duration and the colonic mucosa-associated gut microbiota in humans—a pilot study. Clocks Sleep. 2021;3(3):387–397. doi:10.3390/clockssleep3030025
   PubMedGoogle Scholar
• Lu S, Yang Y, Xu Q, et al. Gut microbiota and targeted biomarkers analysis in patients with cognitive impairment. Front Neurol. 2022;13. doi:10.3389/fneur.2022.834403
   Web of Science ®Google Scholar
• Magzal F, Shochat T, Haimov I, et al. Increased physical activity improves gut microbiota composition and reduces short-chain fatty acid concentrations in older adults with insomnia. Sci Rep. 2022;12(1):2265. doi:10.1038/s41598-022-05099-w
   PubMed Web of Science ®Google Scholar
• Ren T, Gao Y, Qiu Y, et al. Gut microbiota altered in mild cognitive impairment compared with normal cognition in sporadic Parkinson’s disease. Front Neurol. 2020;11:137. doi:10.3389/fneur.2020.00137
   PubMed Web of Science ®Google Scholar
• Vacca M, Celano G, Calabrese FM, Portincasa P, Gobbetti M, De Angelis M. The controversial role of human gut lachnospiraceae. Microorganisms. 2020;8(4):573. doi:10.3390/microorganisms8040573
   PubMed Web of Science ®Google Scholar
• Xu C, Zhu H, Qiu P. Aging progression of human gut microbiota. BMC Microbiol. 2019;19:236. doi:10.1186/s12866-019-1616-2
   PubMed Web of Science ®Google Scholar
• Silva YP, Bernardi A, Frozza RL. The role of short-chain fatty acids from gut microbiota in gut-brain communication. Front Endocrinol. 2020;11. doi:10.3389/fendo.2020.00025
   Web of Science ®Google Scholar
• Smith RP, Easson C, Lyle SM, et al. Gut microbiome diversity is associated with sleep physiology in humans. PLoS One. 2019;14(10):e0222394. doi:10.1371/journal.pone.0222394
   PubMed Web of Science ®Google Scholar