Advertisement

Reviews in Endocrine and Metabolic Disorders

, Volume 20, Issue 4, pp 473–480 | Cite as

Microbiota impacts on chronic inflammation and metabolic syndrome - related cognitive dysfunction

  • María Arnoriaga-Rodríguez
  • José Manuel Fernández-RealEmail author
Article

Abstract

Cognitive dysfunction, one of the major concerns of increased life expectancy, is prevalent in patients with metabolic disorders. Added to the inflammation in the context of aging (inflammaging), low-grade chronic inflammation (metaflammation) accompanies metabolic diseases. Peripheral and central inflammation underlie metabolic syndrome - related cognitive dysfunction. The gut microbiota is increasingly recognized to be linked to both inflammaging and metaflammation in parallel to the pathophysiology of obesity, type 2 diabetes and the metabolic syndrome. Microbiota composition, diversity and diverse metabolites have been related to different metabolic features and cognitive traits. The study of different mouse models has contributed to identify characteristic microbiota profiles and shifts in the microbial gene richness in association with cognitive function. Diet, exercise and prebiotics, probiotics or symbiotics significantly influence cognition and changes in the microbiota. Few studies have analyzed the gut microbiota composition in association with cognitive function in humans. Impaired attention, mental flexibility and executive function have been observed in association with a microbiota ecosystem in cross-sectional and longitudinal studies. Nevertheless, the evidence in humans is still scarce and not causal relationships may be inferred, so larger and long-term studies are required to gain insight into the possible role of microbiota in human cognition.

Keywords

Microbiota Cognitive dysfunction Low-grade inflammation Metabolic disorders 

Notes

Acknowledgments

María Arnoriaga-Rodríguez is funded by a predoctoral “FIS” contract (PI16/02173) from the Instituto de Salud Carlos III, Spain.

Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interest.

Research involving human participants and/or animals. Informed consent

No applicable. This work focused on previously published studies and no own new studies were undertook.

References

  1. 1.
    Institute for Health Metrics and Evaluation [IHME]. Findings from the global burden of disease study 2017. Seattle, WA: IHME; 2018.Google Scholar
  2. 2.
    GBD 2017 DALYs and HALE Collaborators. Global, regional, and national disability-adjusted life-years [DALYs] for 359 diseases and injuries and healthy life expectancy [HALE] for 195 countries and territories, 1990–2017: a systematic analysis for the Global Burden of Diseases Study 2017. Lancet. 2018;392:1859–1922.Google Scholar
  3. 3.
    Sachdev PS, Lipnicki DM, Kochan NA, Crawford JD, Thalamuthu A, Andrews G, et al. The prevalence of mild cognitive impairment in diverse geographical and ethnocultural regions: the COSMIC collaboration. PLoS One. 2015;10:e0142388.PubMedPubMedCentralGoogle Scholar
  4. 4.
    American Psychiatric Association. Diagnostic and statistical manual of mental disorders. 5th ed. Washington DC; 2013.Google Scholar
  5. 5.
    Petersen RC, Smith GE, Waring SC, Ivnik RJ, Kokmen E, Tangelos EG. Aging, memory and mild cognitive impairment. Int Psychogeriatr. 1997;9:65–9.PubMedGoogle Scholar
  6. 6.
    Knopman DS, DeKosky ST, Cummings JL, Chui H, Corey-Bloom J, Relkin N, et al. Practice parameter: diagnosis of dementia [an evidence-based review]. Report of the quality standards Subcommittee of the American Academy of neurology. Neurology. 2001;56:1143–53.PubMedGoogle Scholar
  7. 7.
    Roberts R, Knopman DS. Classification and epidemiology of MCI. Clin Geriatr Med. 2013;29:753–72.PubMedGoogle Scholar
  8. 8.
    Ismail Z, Elbayoumi H, Fischer CE, Hogan DB, Millikin CP, Schweizer T, et al. Prevalence of depression in patients with mild cognitive impairment: a systematic review and meta-analysis. JAMA Psychiatry. 2017;74:58–67.PubMedGoogle Scholar
  9. 9.
    Mirza SS, Ikram MA, Bos D, Mihaescu R, Hofman A, Tiemeir H. Mild cognitive impairment and risk of depression and anxiety: a population-based study. Alzheimers Dement. 2017;13:130–9.PubMedGoogle Scholar
  10. 10.
    Livingston G, Sommerlad A, Orgeta V, Costafreda SG, Huntley J, Ames D, et al. Dementia prevention, intervention and care. Lancet. 2017;390:2673–734.PubMedGoogle Scholar
  11. 11.
    Falony G, Joosens M, Viera-Silva S, Wang J, Darzi Y, Faust K, et al. Population-level analysis of gut microbiome variation. Science. 2016;352:560–4.PubMedGoogle Scholar
  12. 12.
    Nicholson JK, Holmes E, Kinross J, Burcelin R, Gibson G, Jia W, et al. Host-gut microbiota metabolic interactions. Science. 2012;336:1262–7.PubMedPubMedCentralGoogle Scholar
  13. 13.
    Mayer EA. Gut feelings: the emerging biology of gut-brain communication. Nat Rev Neurosci. 2011;12:453–66.PubMedGoogle Scholar
  14. 14.
    Bäckhed F, Fraser CM, Ringel Y, Sanders ME, Sartor RB, Sherman PM, et al. Defining a healthy human gut microbiome: current concepts, future directions, and clinical applications. Cell Host Microbe. 2012;12:611–22.PubMedGoogle Scholar
  15. 15.
    Aziz Q, Doré J, Emmanuel A, Guarner F, Quigley EM. Gut microbiota and gastrointestinal health: current concepts and future directions. Neurogastroenterol Motil. 2013;25:4–15.PubMedGoogle Scholar
  16. 16.
    Biessels GJ, Despa F. Cognitive decline and dementia in diabetes mellitus: mechanisms and clinical implications. Nat Rev Endocrinol. 2018;14:591–604.PubMedPubMedCentralGoogle Scholar
  17. 17.
    O’Brien PD, Hinder LM, Callaghan BC, Fedman EL. Neurological consequences of obesity. Lancet Neurol. 2017;16:465–77.PubMedPubMedCentralGoogle Scholar
  18. 18.
    Farruggia MC, Small DM. Effects of adiposity and metabolic dysfunction on cognition: a review. Physiol Behav. 2019;208:112578.PubMedGoogle Scholar
  19. 19.
    Tilg H, Zmora N, Adolph TE, Elinav E. The intestinal microbiota fuelling metabolic inflammation. Nat Rev Immunol. 2019; 10.1038/s41577-019-0198-4,Google Scholar
  20. 20.
    Pistollato F, Sumalla Cano S, Elio I, Masias Vergara M, Giampieri F, Battino M. Role of gut microbiota and nutrients in amyloid formation and pathogenesis of Alzheimer disease. Nutr Rev. 2016;74:624–34.PubMedGoogle Scholar
  21. 21.
    Alberti KG, Eckel RH, Grundy SM, Zimmet PZ, Cleeman JI, Donato KA, et al. International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; International Association for the Study of Obesity. Circulation. 2009;120:1640–5.PubMedGoogle Scholar
  22. 22.
    O’Neill S, O’Driscoll L. Metabolic syndrome: a closer look at the growing epidemic and its associated pathologies. Obes Rev. 2015;16:1–12.PubMedGoogle Scholar
  23. 23.
    Beydoun MA, Beydoun H, Wang Y. Obesity and central obesity as risk factors for incident dementia and its subtypes: a systematic review and metaanalysis. Obes Rev. 2008;9:204–18.PubMedPubMedCentralGoogle Scholar
  24. 24.
    Pugazhenthi S, Qin L, Reddy PH. Common neurodegenerative pathways in obesity, diabetes, and Alzheimer’s disease. Biochim Biophys Acta Mol basis Dis. 1863;2017:1037–45.Google Scholar
  25. 25.
    Polanco JC, Li C, Bodea LG, Martinez-Marmol R, Meunier FA, Götz J. Amyloid-β and tau complexity-towards improved biomarkers and targeted therapies. Nat Rev Neurol. 2018;14:22–39.PubMedGoogle Scholar
  26. 26.
    Bharadwaj P, Wijesekara N, Liyanapathirana M, Newsholme P, Ittner L, Fraser P, et al. The link between type 2 diabetes and neurodegeneration: roles for amyloid-β, amylin, and tau proteins. J Alzheimers Dis. 2017;59:421–32.PubMedGoogle Scholar
  27. 27.
    Willette AA, Johnson SC, Birdsill AC, Sager MA, Christian B, Baker LD, et al. Insulin resistance predicts brain amyloid deposition in late middle-aged adults. Alzheimers Dement. 2015;11:504–510.e1.PubMedGoogle Scholar
  28. 28.
    Walker JM, Dixit S, Saulsberry AC, May JM, Harrison FE. Reversal of high fat diet-induced obesity improves glucose tolerance, inflammatory response, β-amyloid accumulation and cognitive decline in the APP/PSEN1 mouse model of Alzheimer’s disease. Neurobiol Dis. 2017;100:87–98.PubMedPubMedCentralGoogle Scholar
  29. 29.
    Veronese N, Facchini S, Stubbs B, Luchini C, Solmi M, Manzato E, et al. Weight loss is associated with improvements in cognitive function among overweight and obese people: a systematic review and meta-analysis. Neurosci Biobehav Rev. 2017;72:87–94.PubMedGoogle Scholar
  30. 30.
    Tan CC, Yu JT, Wang HF, Tan MS, Meng XF, Wang C, et al. Efficacy and safety of donepezil, galantamine, rivastigmine, and memantine for the treatment of Alzheimer’s disease: a systematic review and meta-analysis. J Alzheimers Dis. 2014;41:615–31.PubMedGoogle Scholar
  31. 31.
    Consolim-Colombo FM, Sangaleti CT, Costa FO, Morais TL, Lopes HF, Motta JM, et al. Galantamine alleviates inflammation and insulin resistance in patients with metabolic syndrome in a randomized trial. JCI Insight. 2017;2. pii: 93340.Google Scholar
  32. 32.
    Wu Y, Ma Y, Liu Z, Geng Q, Chen Z, Zhang Y. Alterations of myelin morphology and oligodendrocyte development in early stage of Alzheimer’s disease mouse model. Neurosci Lett. 2017;642:102–6.PubMedGoogle Scholar
  33. 33.
    Dean DC 3rd, Hurley SA, Kecskemeti SR, O’Grady JP, Canda C, Davenport-Sis NJ, et al. Association of amyloid pathology with myelin alteration in preclinical Alzheimer disease. JAMA Neurol. 2017;74:41–9.PubMedPubMedCentralGoogle Scholar
  34. 34.
    O’Grady JP, Dean DC 3rd, Yang KL, Canda CM, Hoscheidt SM, Starks EJ, et al. Elevated insulin and insulin resistance are associated with altered myelin in cognitively unimpaired middle-aged adults. Obesity [SilverSpring]. 2019;27:1464–1471.Google Scholar
  35. 35.
    Hotamisligil GS. Inflammation and metabolic disorders. Nature. 2006;444:860–7.PubMedGoogle Scholar
  36. 36.
    King E, O’Brien JT, Donaghy P, Morris C, Barnett N, Olsen K, et al. Peripheral inflammation in prodromal Alzheimer’s and Lewy body dementias. J Neurol Neurosurg Psychiatry. 2018;89:339–45.PubMedGoogle Scholar
  37. 37.
    Wood H. Dementia: peripheral inflammation could be a prodromal indicator of dementia. Nat Rev Neurol. 2018;14:127.PubMedGoogle Scholar
  38. 38.
    Cai D. Neuroinflammation and Neurodegeneration in overnutrition-induced diseases. Trend Endocrinol Metab. 2013;24:40–7.Google Scholar
  39. 39.
    Schain M, Kreisl WC. Neuroinflammation in neurodegenerative disorders - a review. Curr Neurol Neurosci Rep. 2017;17:25.PubMedGoogle Scholar
  40. 40.
    Jais A, Brüning JC. Hypothalamic inflammation in obesity and metabolic disease. J Clin Invest. 2017;127:24–32.PubMedPubMedCentralGoogle Scholar
  41. 41.
    Guillemot-Legris O, Mucciolo GC. Obesity-induced Neuroinflammation: beyond the hypothalamus. Trends Neurosci. 2017;40:237–53.PubMedGoogle Scholar
  42. 42.
    Biessels GJ, Reagan LP. Hippocampal insulin resistance and cognitive dysfunction. Nat Rev Neurosci. 2015;16:660–71.PubMedGoogle Scholar
  43. 43.
    Tracey KJ. The inflammatory reflex. Nature. 2002;420:853–9.PubMedGoogle Scholar
  44. 44.
    Chang EH, Chanvan SS, Pavlov VA. Cholinergic control of inflammation, metabolic dysfunction and cognitive impairment in obesity-associated disorders: mechanism and novel therapeutic opportunities. Front Neurosci. 2019;13:263.PubMedPubMedCentralGoogle Scholar
  45. 45.
    Franceschi C, Garagnani P, Parnin P, Giuliani C, Santoto A. Inflammaging: a new immune-metabolic viewpoint for age-related diseases. Nat Rev Endocrinol. 2018;14:576–90.PubMedGoogle Scholar
  46. 46.
    Deleidi M, Jäggle M, Rubino G. Immune aging, dysmetabolism, and inflammation in neurological diseases. Front Neurosci. 2015;9:172.PubMedPubMedCentralGoogle Scholar
  47. 47.
    Burcelin R. Gut microbiota and immune crosstalk in metabolic disease. Mol Metab. 2016;5:771–81.PubMedPubMedCentralGoogle Scholar
  48. 48.
    Gérard P. Gut microbiota and obesity. Cell Mol Life Sci. 2016;73:147–62.PubMedGoogle Scholar
  49. 49.
    Qin J, Li Y, Cai Z, Li S, Zhu J, Zhang F, et al. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature. 2012;490:55–60.PubMedGoogle Scholar
  50. 50.
    Festi D, Schiumerini R, Henry Eusebi L, Marasco G, Taddia M, Colecchia A. Gut microbiota and metabolic syndrome. World J Gastroenterol. 2014;20:16079–94.PubMedPubMedCentralGoogle Scholar
  51. 51.
    Le Chatelier E, Nielsen T, Qin J, Prifti E, Hildebrand F, Falony G, et al. Richness of human gut microbiome correlates with metabolic markers. Nature. 2013;500:541–6.PubMedPubMedCentralGoogle Scholar
  52. 52.
    Jiang W, Wu N, Wang X, Chi Y, Zhang Y, Qiu X, et al. Dysbiosis gut microbiota associated with inflammation and impaired mucosal immune function in intestine of humans with non-alcoholic fatty liver disease. Sci Rep. 2015;5:8096.PubMedPubMedCentralGoogle Scholar
  53. 53.
    Zweigner J, Schumann RR, Weber JR. The role of lipopolysaccharide-binding protein in modulating the innate immune response. Microbes Infect. 2006;8:946–52.PubMedGoogle Scholar
  54. 54.
    Cani PD, Amar J, Iglesias MA, Poggi M, Knauf C, Bastelica D, et al. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes. 2007;56:1761–72.Google Scholar
  55. 55.
    Moreno-Navarrete JM, Escoté X, Ortega F, Serino M, Campbell M, Michalski MC, et al. A role for adipocyte-derived lipopolysaccharide-binding protein in inflammation- and obesity-associated adipose tissue dysfunction. Diabetologia. 2013;56:2524–37.PubMedGoogle Scholar
  56. 56.
    Hoyles L, Fernández-Real JM, Federici M, Serino M, Abbott J, Charpentier J, et al. Molecular phenomics and metagenomics of hepatic steatosis in non-diabetic obese women. Nat Med. 2018;24:1070–80.PubMedPubMedCentralGoogle Scholar
  57. 57.
    Gribble FM, Reimann F. Function and mechanism of enteroendocrine cells and gut hormones in metabolism. Nat Rev Endocrinol. 2019;15:226–37.PubMedGoogle Scholar
  58. 58.
    Sanna S, van Zuydam NR, Mahajan A, Kurilshikov A, Vich Vila A, Võsa U, et al. Causal relationships among the gut microbiome, short-chain fatty acids and metabolic diseases. Nat Genet. 2019;51:600–5.PubMedPubMedCentralGoogle Scholar
  59. 59.
    Ley RE, Turnbaugh PJ, Klein S, Gordon JI. Microbial ecology: human gut microbes associated with obesity. Nature. 2006;444:1022–3.PubMedGoogle Scholar
  60. 60.
    Gao R, Zhu C, Li H, Yin M, Pan C, Huang L, et al. Dysbiosis signatures of gut microbiota along the sequence from healthy, young patients to those with overweight and obesity. Obesity (Silver Spring). 2018;26:351–61.Google Scholar
  61. 61.
    Debédat J, Clément K, Aron-Wisnewsky J. Gut microbiota dysbiosis in human obesity: impact of bariatric surgery. Curr Obes Rep. 2019;8:229–42.PubMedGoogle Scholar
  62. 62.
    He Y, Wu W, Wu S, Zheng HM, Li P, Sheng HF, et al. Linking gut microbiota, metabolic syndrome and economic status based on a population-level analysis. Microbiome. 2018;6:172.PubMedPubMedCentralGoogle Scholar
  63. 63.
    Tilg H, Moschen AR. Microbiota and diabetes: an evolving relationship. Gut. 2014;63:1513–21.PubMedGoogle Scholar
  64. 64.
    Cani PD, de Vos WM. Next-generation beneficial microbes: the case of Akkermansia muciniphila. Front Microbiol. 2017;8:1765.PubMedPubMedCentralGoogle Scholar
  65. 65.
    Rogers GB, Keating DJ, Young RL, Wong ML, Licinio J, Wesselingh S. From gut dysbiosis to altered brain function and mental illness: mechanisms and pathways. Mol Psychiatry. 2016;21:738–48.PubMedPubMedCentralGoogle Scholar
  66. 66.
    Quigley EMM. Microbiota-brain-gut Axis and neurodegenerative diseases. Curr Neurol Neurosci Rep. 2017;17:94.PubMedGoogle Scholar
  67. 67.
    Liu P, Wu L, Peng G, Han Y, Tang R, Ge J, et al. Altered microbiomes distinguish Alzheimer’s disease from amnestic mild cognitive impairment and health in a Chinese cohort. Brain Behav Immun. 2019;80:633–43.PubMedGoogle Scholar
  68. 68.
    Gao X, Liu X, Xu J, Xue C, Xue Y, Wang Y. Dietary trimethylamine N-oxide exacerbactes impaired glucosa tolerance in mice fed a high fat diet. J Biosci Bioeng. 2014;118:476–81.PubMedGoogle Scholar
  69. 69.
    Dambrova M, Latkovskis G, Kuka J, Strele I, Konrade I, Grinberga S, et al. Diabetes is associated with higher trimethylamine N-oxide plasma levels. Exp Clin Endocrinol Diabetes. 2016;124:251–6.PubMedGoogle Scholar
  70. 70.
    Sanguinetti E, Collado MC, Marrachelli VG, Monleon D, Selma-Royo M, Pardo-Tendero MM, et al. Microbiome-metabolome signatures in mice genetically prone to develop dementia, fed a normal or fatty diet. Sci Rep. 2018;8:4907.PubMedPubMedCentralGoogle Scholar
  71. 71.
    Li D, Ke Y, Zhan R, Liu C, Zhao M, Zeng A, et al. Trimethylamine-N-oxide promotes brain aging and cognitive impairment in mice. Aging Cell. 2018;49:e12768.Google Scholar
  72. 72.
    Vogt NM, Romano KA, Darst BF, Engelman CD, Johnson SC, Carlsson CM, et al. The gut microbiota-derived metabolite trimethylamine N-oxide is elevated in Alzheimer’s disease. Alzheimers Res Ther. 2018;10:124.PubMedPubMedCentralGoogle Scholar
  73. 73.
    Sarkar A, Harty S, Lehto SM, Moeller AH, Dinan TG, Dunbar RIM, et al. The microbiome in psychology and cognitive neuroscience. Trends Cogn Sci. 2018;22:611–36.PubMedGoogle Scholar
  74. 74.
    Yang Y, Zhong Z, Wang B, Xia X, Yao W, Huang L, et al. Early-life high-fat diet-induced obesity programs hippocampal development and cognitive functions via regulation of gut commensal Akkermansia muciniphila. Neuropsychopharmacology. 2019;44:2054–64.PubMedGoogle Scholar
  75. 75.
    Everard A, Belzer C, Geurts L, Ouwerkerk JP, Druart C, Bindels LB, et al. Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc Natl Acad Sci U S A. 2013;110:9066–71.PubMedPubMedCentralGoogle Scholar
  76. 76.
    Kang SS, Jeraldo PR, Kurti A, Miller ME, Cook MD, Whitlock K, et al. Diet and exercise orthogonally alter the gut microbiome and reveal independent associations with anxiety and cognition. Mol Neurodegener. 2014;9:36.PubMedPubMedCentralGoogle Scholar
  77. 77.
    Zhang P, Yu Y, Qin Y, Zhou Y, Tang R, Wang Q, et al. Alterations to the microbiota-colon-brain axis in high-fat-diet-induced obese mice compared to diet-resistant mice. J Nutr Biochem. 2019;65:54–65.PubMedGoogle Scholar
  78. 78.
    Jena PK, Sheng L, Di Lucente J, Jin LW, Maezawa I, Wan YY. Dysregulated bile acid synthesis and dysbiosis are implicated in Western diet-induced systemic inflammation, microglial activation, and reduced neuroplasticity. FASEB J. 2018;32:2866–77.PubMedPubMedCentralGoogle Scholar
  79. 79.
    Magnusson KR, Hauck L, Jeffrey BM, Elias V, Humphrey A, Nath R, et al. Relationships between diet-related changes in the gut microbiome and cognitive flexibility. Neuroscience. 2015;300:128–40.PubMedGoogle Scholar
  80. 80.
    Liu Z, Yuan T, Dai X, Shi L, Liu X. Intermittent fasting alleviates diabetes-induced cognitive decline via gut microbiota-metabolites-brain axis [OR32–04-19]. Curr Dev Nutr. 2019;3:nzz052.  https://doi.org/10.1093/cdn/nzz052.OR32-04-19.CrossRefPubMedCentralGoogle Scholar
  81. 81.
    Marungruang N, Kovalenko T, Osadchenko I, Voss U, Huang F, Burleigh S, et al. Lingonberries and their two separated fractions differently alter the gut microbiota, improve metabolic functions, reduce gut inflammatory properties, and improve brain function in ApoE−/− mice fed high-fat diet. Nutr Neurosci. 2018:1–13.Google Scholar
  82. 82.
    López P, Sánchez M, Pérez-Cruz C, Velázquez-Villegas LA, Syeda T, Aguilar-López M, et al. Long-term genistein consumption modifies gut microbiota, improving glucose metabolism, metabolic endotoxemia, and cognitive function in mica fed a high-fat diet. Mol Nutr Food Res. 2018;62:e1800313.PubMedGoogle Scholar
  83. 83.
    Lv M, Yang S, Cai L, Qin LQ, Li BY, Wan Z. Effects of quercetin intervention on cognition function in APP/PS1 mice was affected by vitamin D status. Mol Nutr Food Res. 2018;62:e1800621.PubMedGoogle Scholar
  84. 84.
    Chunchai T, Thunapong W, Yasom S, Wanchai K, Eaimworawuthikul S, Metzler G, et al. Decreased microglial activation through gut-brain axis by prebiotics, probiotics, or symbiotics effectively restored cognitive function in obese-insulin resistant rats. J Neuroinflammation. 2018;15:11.PubMedPubMedCentralGoogle Scholar
  85. 85.
    Fernández-Real JM, Serino M, Blasco G, Puig J, Daunis-i-Estadella J, Ricart W, et al. Gut microbiota interacts with brain microstructure and function. J Clin Endocrinol Metab. 2015;100:4505–13.PubMedGoogle Scholar
  86. 86.
    Meadowcroft MD, Peters DG, Dewal RP, Connor JR, Yang QX. The effect of iron in MRI and transverse relaxation of amyloid-beta plaques in Alzheimer’s disease. NMR Biomed. 2015;28:297–305.PubMedGoogle Scholar
  87. 87.
    Palomo-Buitrago ME, Sabater-Masdeu M, Moreno-Navarrete JM, Caballano-Infantes E, Arnoriaga-Rodríguez M, Coll C, et al. Glutamate interactions with obesity, insulin resistance, cognition and gut microbiota composition. Acta Diabetol. 2019;56:569–79.PubMedGoogle Scholar
  88. 88.
    Anderson JR, Carroll I, Azcarate-Peril MA, Rochette AD, Heinberg LJ, Peat C, et al. A preliminary examination of gut microbiota, sleep, and cognitive flexibility in healthy older adults. Sleep Med. 2017;38:104–7.PubMedGoogle Scholar
  89. 89.
    Blasco G, Moreno-Navarrete JM, Rivero M, Pérez-Brocal V, Garre-Olmo J, Puig J, et al. The gut metagenome changes in parallel to waist circumference, brain iron deposition, and cognitive function. J Clin Endocrinol Metab. 2017;102:2962–73.PubMedGoogle Scholar
  90. 90.
    Janelidze S, Stomrud E, Palmqvist S, Zetterberg H, van Western D, Jeromin A, et al. Plasma β-amyloid in Alzheimer’s disease and vascular disease. Sci Rep. 2016;6:26801.PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Diabetes, Endocrinology and NutritionDr. Josep Trueta University Hospital, Girona Biomedical Research Institute [IdibGi]GironaSpain
  2. 2.Nutrition, Eumetabolism and Health GroupGirona Biomedical Research Institute (IdibGi)GironaSpain
  3. 3.CIBEROBN Physiopathology of Obesity and Nutrition (CIBEROBN)MadridSpain
  4. 4.Department of Medical Sciences, Faculty of MedicineUniversity of GironaGironaSpain

Personalised recommendations