AI Chat Paper
Note: Please note that the following content is generated by AMiner AI. SciOpen does not take any responsibility related to this content.
{{lang === 'zh_CN' ? '文章概述' : 'Summary'}}
{{lang === 'en_US' ? '中' : 'Eng'}}
Chat more with AI
Powered by AMiner. Clicking this button will take you away from SciOpen.
Home Food Science and Human Wellness Article
PDF (1.3 MB)
Cite
EndNote(RIS) BibTeX
Collect
Submit Manuscript AI Chat Paper
Show Outline
Outline
Show full outline
Hide outline
Outline
Show full outline
Hide outline
Open Access

Microbial phenolic metabolites are associated with better frontal lobe cognition

Inés Domínguez-Lópeza,b,c,1, Isabella Parilli-Mosera,b,c,1, Anna Vallverdú-Queralta,b,c, Anna Tresserra-Rimbaua,b,c, Cinta Valls-Pedretc,d, Zenaida Vázquez-Ruizc,e, Olga Castañerc,f, Ramon Estruchc,g, Emili Rosc,h, Rosa M. Lamuela-Raventósa,b,c( )
Departament de Nutrició, Ciències de l’Alimentació i Gastronomía, Facultat de Farmacia, Universitat de Barcelon (UB), Barcelona 08028, Spain
Institut de Nutrició i Seguretat Alimentària (INSA), Universitat de Barcelona (UB), Santa Coloma de Gramanet 08034, Spain
CIBER Fisiopatología de la Obesidad y Nutrición (CIBEROBN), Instituto de Salud Carlos Ⅲ, Madrid 28029, Spain
Lipid Clinic, Endocrinology and Nutrition Service, Institut d'Investigacions Biomèdiques August Pi i Sunyer, Hospital Clínic, Barcelona 08036, Spain
Department of Preventive Medicine and Public Health, University of Navarra, IdiSNA, Pamplona 31008, Spain
Unit of Cardiovascular Risk and Nutrition, Institut Hospital del Mar de Investigaciones Médicas (IMIM), Barcelona 08007, Spain
Department of Internal Medicine, Hospital Clinic, Institut d’Investigació Biomèdica August Pi i Sunyer (IDIBAPS), University of Barcelona, Barcelona 08007, Spain
Department of Endocrinology, Hospital Clinic, IDIBAPS, Barcelona 08007, Spain

1 Equally contributing authors.

Peer review under responsibility of Tsinghua University Press.

Show Author Information

Abstract

With increasing life expectancy, neurodegenerative diseases have become one of the leading causes of ill-health in the elderly. Preventive strategies include following healthy diets, such as the Mediterranean diet, which is particularly rich in polyphenols, bioactive compounds with neuroprotective properties. The aim of this study was to assess the association of microbial phenolic metabolites (MPM) with cognition. This cross-sectional analysis was performed with 200 participants of the PREDIMED trial (Barcelona-Clinic recruitment center). A novel method based on liquid chromatography coupled to mass spectrometry was used to identify urinary MPM (protocatechuic acid, enterodiol glucuronide, enterolactone glucuronide, urolithin B glucuronide, and vanillic acid glucuronide), and cognitive function was evaluated with neuropsychological tests. Multivariable-adjusted ordinary least squares regression was used to assess the associations between cognitive function and MPM, and a score was calculated as the weighted sum of MPM. A higher MPM score was associated with better frontal lobe function. Among individual metabolites, vanillic acid glucuronide was correlated with frontal cognitive performance. Participants with higher concentrations of vanillic acid glucuronide and urolithin B glucuronide obtained better scores in the Color Trail Test part 2. A higher score for urinary multi-MPM was associated with better frontal cognitive performance in an older Mediterranean population.

Keywords

PolyphenolsNeurodegenerationMicrobiotaGut-brain axisPREDIMED

Electronic Supplementary Material

Download File(s)
fshw-13-6-3266_ESM.docx (18.8 KB)

References

[1]

G.A. Roth, D. Abate, K.H. Abate, et al., Global, regional, and national age-sex-specific mortality for 282 causes of death in 195 countries and territories, 1980–2017: a systematic analysis for the Global Burden of Disease Study 2017, Lancet 392 (2018) 1736-1788. https://doi.org/10.1016/S0140-6736(18)32203-7.
Crossref Google Scholar
[2]

H. Niu, I. Álvarez-Álvarez, F. Guillén-Grima, et al., Prevalencia e incidencia de la enfermedad de Alzheimer en Europa: metaanálisis, Neurologia 32 (2017) 523-532. https://doi.org/10.1016/j.nrl.2016.02.016.
Crossref Google Scholar
[3]

C.A. Lane, J. Hardy, J.M. Schott, Alzheimer’s disease, Eur. J. Neurol. 25 (2018) 59-70. https://doi.org/10.1111/ene.13439.
Crossref Google Scholar
[4]

M. Baumgart, H.M. Snyder, M.C. Carrillo, et al., Summary of the evidence on modifiable risk factors for cognitive decline and dementia: a population-based perspective, Alzheimer’s Dement. 11 (2015) 718-726. https://doi.org/10.1016/j.jalz.2015.05.016.
Crossref Google Scholar
[5]

N. Scarmeas, C.A. Anastasiou, M. Yannakoulia, Nutrition and prevention of cognitive impairment, Lancet Neurol. 17 (2018) 1006-1015. https://doi.org/10.1016/S1474-4422(18)30338-7.
Crossref Google Scholar
[6]

D.G. Loughrey, S. Lavecchia, S. Brennan, et al., The impact ofsocial activities, social networks, social support and social relationships on the cognitive functioning of healthy older adults: a systematic review, Syst. Rev. 8 (2017) 571-586. https://doi.org/10.1186/s13643-017-0632-2.
Crossref Google Scholar
[7]

J. Barbaresko, A.W. Lellmann, A. Schmidt, et al., Dietary factors and neurodegenerative disorders: an umbrella review of meta-analyses of prospective studies, Adv. Nutr. 11 (2020) 1161-1173. https://doi.org/10.1093/advances/nmaa053.
Crossref Google Scholar
[8]

A. Bach-Faig, E.M. Berry, D. Lairon, et al., Mediterranean diet pyramid today. Science and cultural updates, Public Health Nutr. 14 (2011) 2274. https://doi.org/10.1017/S1368980011002515.
Crossref Google Scholar
[9]

M. Steele, G. Stuchbury, G. Münch, The molecular basis of the prevention of Alzheimer’s disease through healthy nutrition, Exp. Gerontol. 42 (2007) 28-36. https://doi.org/10.1016/j.exger.2006.06.002.
Crossref Google Scholar
[10]

C. Valls-Pedret, R.M. Lamuela-Raventós, A. Medina-Remón, et al., Polyphenol-rich foods in the mediterranean diet are associated with better cognitive function in elderly subjects at high cardiovascular risk, J. Alzheimer’s Dis. 29 (2012) 773-782. https://doi.org/10.3233/JAD-2012-111799.
Crossref Google Scholar
[11]

F. Cardona, C. Andrés-Lacueva, S. Tulipani, et al., Benefits of polyphenols on gut microbiota and implications in human health, J. Nutr. Biochem. 24 (2013) 1415-1422. https://doi.org/10.1016/j.jnutbio.2013.05.001.
Crossref Google Scholar
[12]

S. Filosa, F. Di Meo, S. Crispi, Polyphenols-gut microbiota interplay and brain neuromodulation, Neural Regen. Res. 13 (2018) 2055-2059. https://doi.org/10.4103/1673-5374.241429.
Crossref Google Scholar
[13]

M.Á. Martínez-González, D. Corella, J. Salas-salvadó, et al., Cohort profile: design and methods of the PREDIMED study, Int. J. Epidemiol. 41 (2012) 377-385. https://doi.org/10.1093/ije/dyq250.
Crossref Google Scholar
[14]

R. Estruch, M.A. Martínez-González, D. Corella, et al., Annals of internal medicine article effects of a mediterranean-style diet on cardiovascular risk factors, Ann. Intern. Med. 145 (2006) 1-11.
Crossref Google Scholar
[15]

C. Valls-Pedret, A. Sala-Vila, M. Serra-Mir, et al., Mediterranean diet and age-related cognitive decline: a randomized clinical trial, JAMA Intern. Med. 175 (2015) 1094-1103. https://doi.org/10.1001/jamainternmed.2015.1668.
Crossref Google Scholar
[16]

W.C. Willett, Nutritional Epidemiology, Oxford University Press, New York, USA, 2012. https://doi.org/10.1093/acprof:oso/9780199754038.001.0001.
Crossref
[17]

J.D. Fernández-Ballart, J.L. Piñol, I. Zazpe, et al., Relative validity of a semi-quantitative food-frequency questionnaire in an elderly Mediterranean population of Spain, Br. J. Nutr. 103 (2010) 1808. https://doi.org/10.1017/S0007114509993837.
Crossref Google Scholar
[18]

R. Elosua, M. Garcia, A. Aguilar, et al., Validation of the minnesota leisure time Spanish women, Med. Sci. Sport. Exerc. 32 (2000) 1431-1437.
Crossref Google Scholar
[19]

M. Folstein, S. Folstein, “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician, J. Psychiatr. Res. 12 (1975) 189-198. https://doi.org/10.3744/snak.2003.40.2.021.
Crossref Google Scholar
[20]

A. Rey, L’examen Clinique en Psychologie, Paris, 1964.
[21]

D. Wechsler, A standardized memory scale for clinical use, J. Psychol. 19 (1945) 87-95.
Crossref Google Scholar
[22]

A. Ramier, H. Hecaen, Role respectif des atteintes frontales et de la lateralisation lésionnelle dans les déficits de la fluence verbale, Rev. Neurol. 123 (1970) 17-22.
Google Scholar
[23]

D. Wechsler, Escala de inteligencia de Wechsler para adultos-Ⅲ (WAIS Ⅲ), Madrid, 1999.
[24]

L. D’Elia, P. Satz, C. Uchiyama, T. White, Color trails: professional manual, Odessa, 1994.
[25]

E.P. Laveriano-santos, M. Marhuenda-muñoz, A. Vallverd, et al., Identification and quantification of urinary microbial phenolic metabolites by HPLC-ESI-LTQ-Orbitrap-HRMS and their relationship with dietary polyphenols in adolescents, Antioxidants 11(6) (2022) 1167. https://doi.org/10.3390/antiox11061167.
Crossref Google Scholar
[26]

A. Medina-Remón, A. Barrionuevo-González, R. Zamora-Ros, et al., Rapid Folin-Ciocalteu method using microtiter 96-well plate cartridges for solid phase extraction to assess urinary total phenolic compounds, as a biomarker of total polyphenols intake, Anal. Chim. Acta 634 (2009) 54-60. https://doi.org/10.1016/j.aca.2008.12.012.
Crossref Google Scholar
[27]

G. Blom, Statistical estimates and transformed beta variables, Inc. Stat. 10 (1960) 53-55. https://doi.org/10.2307/2987488.
Crossref Google Scholar
[28]

R.E. Ley, C.A. Lozupone, M. Hamady, et al., Worlds within worlds: evolution of the vertebrate gut microbiota, Nat. Rev. Microbiol. 6 (2008) 776-788. https://doi.org/10.1038/nrmicro1978.
Crossref Google Scholar
[29]

J. Godos, F. Caraci, A. Micek, et al., Dietary phenolic acids and their major food sources are associated with cognitive status in older Italian adults, Antioxidants 10 (2021) 1-11. https://doi.org/10.3390/antiox10050700.
Crossref Google Scholar
[30]

N. Cheng, L. Bell, D.J. Lamport, et al., Dietary flavonoids and human cognition: a meta-analysis, Mol. Nutr. Food Res. 2100976 (2022) 1-15. https://doi.org/10.1002/mnfr.202100976.
Crossref Google Scholar
[31]

R. González-Domínguez, P. Castellano-Escuder, F. Carmona, et al., Food and microbiota metabolites associate with cognitive decline in older subjects: a 12-year prospective study, Mol. Nutr. Food Res. 65 (2021) 1-10. https://doi.org/10.1002/mnfr.202100606.
Crossref Google Scholar
[32]

K. Krzysztoforska, D. Mirowska-Guzel, E. Widy-Tyszkiewicz, Pharmacological effects of protocatechuic acid and its therapeutic potential in neurodegenerative diseases: review on the basis of in vitro and in vivo studies in rodents and humans, Nutr. Neurosci. 22 (2019) 72-82. https://doi.org/10.1080/1028415X.2017.1354543.
Crossref Google Scholar
[33]

D. Wang, L. Ho, J. Faith, et al., Role of intestinal microbiota in the generation of polyphenol-derived phenolic acid mediated attenuation of Alzheimer’s disease β-amyloid oligomerization, Mol. Nutr. Food Res. 59 (2015) 1025-1040. https://doi.org/10.1002/mnfr.201400544.
Crossref Google Scholar
[34]

B.S. McEwen, J.H. Morrison, The brain on stress: vulnerability and plasticity of the prefrontal cortex over the life course, Neuron. 79 (2013) 16-29. https://doi.org/10.1016/j.neuron.2013.06.028.
Crossref Google Scholar
[35]

N.S. Vigliecca, S. Baez, Screening executive function and global cognition with the Nine-Card Sorting Test: healthy participant studies and ageing implications, Psychogeriatrics 15 (2015) 163-170. https://doi.org/10.1111/psyg.12104.
Crossref Google Scholar
[36]

R. Kean, D. Lamport, J. Ellis, et al., Chronic consumption of orange juice flavonoids is associated with cognitive benefits: an 8 week randomised double-blind placebo-controlled trial in older adults, Appetite 130 (2018) 308. https://doi.org/10.1016/j.appet.2018.05.204.
Crossref Google Scholar
[37]

A.B. Scholey, S.J. French, P.J. Morris, et al., Consumption of cocoa flavanols results in acute improvements in mood and cognitive performance during sustained mental effort, J. Psychopharmacol. 24 (2010) 1505-1514. https://doi.org/10.1177/0269881109106923.
Crossref Google Scholar
[38]

K. de Vries, E. Medawar, A. Korosi, et al., The effect of polyphenols on working and episodic memory in non-pathological and pathological aging: a systematic review and meta-analysis, Front. Nutr. 8 (2022). https://doi.org/10.3389/fnut.2021.720756.
Crossref Google Scholar
[39]

F. Sarubbo, D. Moranta, G. Pani, Dietary polyphenols and neurogenesis: molecular interactions and implication for brain ageing and cognition, Neurosci. Biobehav. Rev. 90 (2018) 456-470. https://doi.org/10.1016/j.neubiorev.2018.05.011.
Crossref Google Scholar
[40]

V. Castelli, D. Grassi, R. Bocale, et al., Diet and brain health: which role for polyphenols? Curr. Pharm. Des. 24 (2017) 227-238. https://doi.org/10.2174/1381612824666171213100449.
Crossref Google Scholar
[41]

I. Hajjar, S.S. Hayek, F.C. Goldstein, et al., Oxidative stress predicts cognitive decline with aging in healthy adults: an observational study, J. Neuroinflamm. 15 (2018) 1-7. https://doi.org/10.1186/s12974-017-1026-z.
Crossref Google Scholar
[42]

N. Raz, K.M. Rodrigue, J.D. Acker, Hypertension and the brain: vulnerability of the prefrontal regions and executive functions, Behav. Neurosci. 117 (2003) 1169-1180. https://doi.org/10.1037/0735-7044.117.6.1169.
Crossref Google Scholar
[43]

J. Tan, Y. Li, D.X. Hou, et al., The effects and mechanisms of cyanidin-3-glucoside and its phenolic metabolites in maintaining intestinal integrity, Antioxidants 8 (2019) 1-16. https://doi.org/10.3390/antiox8100479.
Crossref Google Scholar
[44]

L. Bell, D.J. Lamport, L.T. Butler, et al., A review of the cognitive effects observed in humans following acute supplementation with flavonoids, and their associated mechanisms of action, Nutrients 7 (2015) 10290-10306. https://doi.org/10.3390/nu7125538.
Crossref Google Scholar
[45]

N. Ahmadi, N. Mirazi, A. Komaki, et al., Vanillic acid attenuates amyloid β1-40-induced long-term potentiation deficit in male rats: an in vivo investigation, Neurol. Res. 43 (2021) 562-569. https://doi.org/10.1080/01616412.2021.1893565.
Crossref Google Scholar
[46]

N. Ahmadi, S. Safari, N. Mirazi, et al., Effects of vanillic acid on Aβ1-40-induced oxidative stress and learning and memory deficit in male rats, Brain Res. Bull. 170 (2021) 264-273. https://doi.org/10.1016/j.brainresbull.2021.02.024.
Crossref Google Scholar
[47]

V.F. Salau, O.L. Erukainure, C.U. Ibeji, et al., Vanillin and vanillic acid modulate antioxidant defense system via amelioration of metabolic complications linked to Fe2+-induced brain tissues damage, Metab. Brain Dis. 35 (2020) 727-738. https://doi.org/10.1007/s11011-020-00545-y.
Crossref Google Scholar
[48]

R. Ullah, M. Ikram, T.J. Park, et al., Vanillic acid, a bioactive phenolic compound, counteracts LPS-induced neurotoxicity by regulating c-jun n-terminal kinase in mouse brain, Int. J. Mol. Sci. 22 (2021) 1-21. https://doi.org/10.3390/ijms22010361.
Crossref Google Scholar
[49]

A. López-Yerena, I. Domínguez-López, A. Vallverdú-Queralt, et al., Metabolomics technologies for the identification and quantification of dietary phenolic compound metabolites: an overview, Antioxidants 10 (2021) 1-25. https://doi.org/10.3390/antiox10060846.
Crossref Google Scholar
[50]

G. Lee, J.S. Park, E.J. Lee, et al., Anti-inflammatory and antioxidant mechanisms of urolithin B in activated microglia, Phytomedicine 55 (2019) 50-57. https://doi.org/10.1016/j.phymed.2018.06.032.
Crossref Google Scholar
[51]

P. Chen, F. Chen, J. Lei, et al., The gut microbiota metabolite urolithin b improves cognitive deficits by inhibiting Cyt C-mediated apoptosis and promoting the survival of neurons through the PI3K pathway in aging mice, Front. Pharmacol. 12 (2021) 1-21. https://doi.org/10.3389/fphar.2021.768097.
Crossref Google Scholar
[52]

I. Figueira, G. Garcia, R.C. Pimpão, et al., Polyphenols journey through blood-brain barrier towards neuronal protection, Sci. Rep. 7 (2017) 1-16. https://doi.org/10.1038/s41598-017-11512-6.
Crossref Google Scholar
Food Science and Human Wellness
Volume 13 Issue 6,
November 2024
Pages 3266-3272
DOI: 10.26599/FSHW.2023.9250013
Cite this article:
Domínguez-López I, Parilli-Moser I, Vallverdú-Queralt A, et al. Microbial phenolic metabolites are associated with better frontal lobe cognition. Food Science and Human Wellness, 2024, 13(6): 3266-3272. https://doi.org/10.26599/FSHW.2023.9250013

578

Views

68

Downloads

0

Crossref

0

Web of Science

0

Scopus

0

CSCD

Altmetrics
Received: 14 July 2022
Revised: 15 September 2022
Accepted: 14 October 2022
Published: 18 December 2024
© 2024 Beijing Academy of Food Sciences. Publishing services by Tsinghua University Press.

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Return