The acute effect of flavonoid-rich apples and nitrate-rich spinach on cognitive performance and mood in healthy men and women

Food and Function

Volumn 5, Issue 5, 2014, Pages 849-858

  Bondonno, Catherine P ^a   Downey, Luke A ^b,c   Croft, Kevin D ^a   Scholey, Andrew ^b   Stough, Con ^b   Yang, Xingbin ^d   Considine, Michael J ^e,f   Ward, Natalie C ^a   Puddey, Ian B ^a   Swinny, Ewald ^g   Mubarak, Aidilla ^a,e,h   Hodgson, Jonathan M ^a  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^b SWINBURNE UNIVERSITY OF TECHNOLOGY   (Australia)

^c SWANSEA UNIVERSITY   (United Kingdom)

^d SHAANXI NORMAL UNIVERSITY   (China)

^e UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^f DEPARTMENT OF AGRICULTURE AND FOOD WESTERN AUSTRALIA   (Australia)

^g Chemistry Centre Western Australia   (Australia)

^h UNIVERSITI MALAYSIA TERENGGANU   (Malaysia)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN; FLAVONOIDS; FRUITS; NITRIC OXIDE; PLASMAS;

CARDIO-VASCULAR DISEASE; COGNITIVE ASSESSMENTS; COGNITIVE DECLINE; COGNITIVE FUNCTIONS; COGNITIVE PERFORMANCE; DRUG RESEARCH; FRUIT AND VEGETABLES; S-NITROSOTHIOLS;

NITRATES;

FLAVONOID; NITRIC ACID DERIVATIVE;

ADULT; AFFECT; CHEMISTRY; COGNITION; CONTROLLED STUDY; FEMALE; HUMAN; MALE; MALUS; METABOLISM; MIDDLE AGED; RANDOMIZED CONTROLLED TRIAL; SPINACH; YOUNG ADULT;

ADULT; AFFECT; COGNITION; FEMALE; FLAVONOIDS; HUMANS; MALE; MALUS; MIDDLE AGED; NITRATES; SPINACIA OLERACEA; YOUNG ADULT;

EID: 84899585246     PISSN: 20426496     EISSN: 2042650X     Source Type: Journal    
DOI: 10.1039/c3fo60590f     Document Type: Article

References (73)

1. L. A. Bazzano M. K. Serdula S. Liu Dietary intake of fruits and vegetables and risk of cardiovascular disease Curr. Atheroscler. Rep. 2003 5 492 499
2. A. R. Ness J. W. Powles Fruit and vegetables, and cardiovascular disease: a review Int. J. Epidemiol. 1997 26 1 13
3. P. van't Veer M. C. Jansen M. Klerk F. J. Kok Fruits and vegetables in the prevention of cancer and cardiovascular disease Public Health Nutr. 2000 3 103 107
4. C. Feart C. Samieri P. Barberger-Gateau Mediterranean diet and cognitive function in older adults Curr. Opin. Clin. Nutr. Metab. Care 2010 13 14
5. J. H. Kang A. Ascherio F. Grodstein Fruit and vegetable consumption and cognitive decline in aging women Ann. Neurol. 2005 57 713 720
6. R. O. Roberts Y. E. Geda J. R. Cerhan D. S. Knopman R. H. Cha T. J. H. Christianson V. S. Pankratz R. J. Ivnik B. F. Boeve H. M. O'Connor Vegetables, unsaturated fats, moderate alcohol intake, and mild cognitive impairment Dementia Geriatr. Cognit. Disord. 2010 29 413 423
7. W. M. Loke J. M. Hodgson J. M. Proudfoot A. J. McKinley I. B. Puddey K. D. Croft Pure dietary flavonoids quercetin and (-)-epicatechin augment nitric oxide products and reduce endothelin-1 acutely in healthy men Am. J. Clin. Nutr. 2008 88 1018 1025
8. J. O. Lundberg M. Govoni Inorganic nitrate is a possible source for systemic generation of nitric oxide Free Radical Biol. Med. 2004 37 395 400
9. R. C. Jin J. Loscalzo Vascular nitric oxide: formation and function J. Blood Med. 2010 1 147 162
10. K. K. K. Chung K. K. David Emerging roles of nitric oxide in neurodegeneration Nitric Oxide 2010 22 290 295
11. R. Schulz T. Rassaf P. B. Massion M. Kelm J. L. Balligand Recent advances in the understanding of the role of nitric oxide in cardiovascular homeostasis Pharmacol. Ther. 2005 108 225 256
12. L. J. Launer Demonstrating the case that AD is a vascular disease: epidemiologic evidence Ageing Res. Rev. 2002 1 61 77
13. P. M. Rhodes A. M. Leone P. L. Francis A. D. Struthers S. Moncada The l-arginine: nitric oxide pathway is the major source of plasma nitrite in fasted humans Biochem. Biophys. Res. Commun. 1995 209 590 596
14. C. Heiss A. Dejam P. Kleinbongard T. Schewe H. Sies M. Kelm Vascular effects of cocoa rich in flavan-3-ols JAMA 2003 290 1030 1031
15. H. Schroeter C. Heiss J. Balzer P. Kleinbongard C. L. Keen N. K. Hollenberg H. Sies C. Kwik-Uribe H. H. Schmitz M. Kelm (-)-Epicatechin mediates beneficial effects of flavanol-rich cocoa on vascular function in humans Proc. Natl. Acad. Sci. U. S. A. 2006 103 1024 1029
16. M. Govoni E. A. Jansson E. Weitzberg J. O. Lundberg The increase in plasma nitrite after a dietary nitrate load is markedly attenuated by an antibacterial mouthwash Nitric Oxide 2008 19 333 337
17. J. Petersson M. Carlström O. Schreiber M. Phillipson G. Christoffersson A. Jägare S. Roos E. Å. Jansson A. E. G. Persson J. O. Lundberg L. Holm Gastroprotective and blood pressure lowering effects of dietary nitrate are abolished by an antiseptic mouthwash Free Radical Biol. Med. 2009 46 1068 1075
18. A. J. Webb N. Patel S. Loukogeorgakis M. Okorie Z. Aboud S. Misra R. Rashid P. Miall J. Deanfield N. Benjamin R. MacAllister A. J. Hobbs A. Ahluwalia Acute blood pressure lowering, vasoprotective, and antiplatelet properties of dietary nitrate via bioconversion to nitrite Hypertension 2008 51 784 790
19. C. P. Bondonno X. Yang K. D. Croft M. J. Considine N. C. Ward L. Rich I. B. Puddey E. Swinny A. Mubarak J. M. Hodgson Flavonoid-rich apples and nitrate-rich spinach augment nitric oxide status and improve endothelial function in healthy men and women: a randomized controlled trial Free Radical Biol. Med. 2012 52 95 102
20. J. A. Gally P. R. Montague G. N. Reeke Jr G. M. Edelman The NO hypothesis: possible effects of a short-lived, rapidly diffusible signal in the development and function of the nervous system Proc. Natl. Acad. Sci. U. S. A. 1990 87 3547 3551
21. A. B. Knott E. Bossy-Wetzel Nitric oxide in health and disease of the nervous system Antioxid. Redox Signaling 2009 11 541 553
22. P. Knekt S. Isotupa Quercetin intake and the incidence of cerebrovascular disease Eur. J. Clin. Nutr. 2000 54 415
23. H. D. Sesso J. M. Gaziano S. Liu J. E. Buring Flavonoid intake and the risk of cardiovascular disease in women Am. J. Clin. Nutr. 2003 77 1400 1408
24. A. Petersen S. Stoltze Nitrate and nitrite in vegetables on the Danish market: content and intake Food Addit. Contam. 1999 16 291 299
25. G. Ysart P. Miller G. Barrett D. Farrington P. Lawrance N. Harrison Dietary exposures to nitrate in the UK Food Addit. Contam. 1999 16 521 532
26. B. Gago J. O. Lundberg R. M. Barbosa J. Laranjinha Red wine-dependent reduction of nitrite to nitric oxide in the stomach Free Radical Biol. Med. 2007 43 1233 1242
27. L. Peri D. Pietraforte G. Scorza A. Napolitano V. Fogliano M. Minetti Apples increase nitric oxide production by human saliva at the acidic pH of the stomach: a new biological function for polyphenols with a catechol group? Free Radical Biol. Med. 2005 39 668 681
28. B. S. Rocha B. Gago R. M. Barbosa J. Laranjinha Diffusion of nitric oxide through the gastric wall upon reduction of nitrite by red wine: physiological impact Nitric Oxide 2010 22 235 241
29. K. A. Wesnes T. Ward G. Ayre C. Pincock Validity and utility of the cognitive drug research (CDR) computerised cognitive testing system: a review following fifteen years of usage Eur. Neuropsychopharmacol. 1999 9 368
30. C. Manach G. Williamson C. Morand A. Scalbert C. Remesy Bioavailability and bioefficacy of polyphenols in humans. I. Review of 97 bioavailability studies Am. J. Clin. Nutr. 2005 81 230S 242S
31. J. Lee A. E. Mitchell Pharmacokinetics of quercetin absorption from apples and onions in healthy humans J. Agric. Food Chem. 2012 60 3874 3881
32. D. L. Granger, N. M. Anstey, W. C. Miller, J. B. Weinberg and P. Lester, in Methods Enzymol, Academic Press, 1999, vol. 31, pp. 49-61
33. F. A. Tomas-Barberan M. I. Gil P. Cremin A. L. Waterhouse B. Hess-Pierce A. A. Kader HPLC-DAD-ESIMS analysis of phenolic compounds in nectarines, peaches, and plums J. Agric. Food Chem. 2001 49 4748 4760
34. X. Yang C. P. Bondonno A. Indrawan J. M. Hodgson K. D. Croft An Improved Mass Spectrometry Based Measurement Of No Metabolites In Biological Fluids Free Radical Biol. Med. 2013 56 1 8
35. J. Ryan K. Croft T. Mori K. Wesnes J. Spong L. Downey C. Kure J. Lloyd C. Stough An examination of the effects of the antioxidant Pycnogenol on cognitive performance, serum lipid profile, endocrinological and oxidative stress biomarkers in an elderly population J. Psychopharmacol. 2008 22 553 562
36. C. Stough L. A. Downey J. Lloyd B. Silber S. Redman C. Hutchison K. Wesnes P. J. Nathan Examining the nootropic effects of a special extract of Bacopa monniera on human cognitive functioning: 90 day double-blind placebo-controlled randomized trial Phytother. Res. 2008 22 1629 1634
37. K. Wesnes T. Ward A. McGinty O. Petrini The memory enhancing effects of a Ginkgo biloba/Panax ginseng combination in healthy middle-aged volunteers Psychopharmacology 2000 152 353 361
38. D. Kennedy C. Haskell K. Wesnes A. Scholey Improved cognitive performance in human volunteers following administration of guarana (Paullinia cupana) extract: comparison and interaction with Panax ginseng Pharmacol., Biochem. Behav. 2004 79 401 411
39. A. Bond M. Lader The use of analogue scales in rating subjective feelings Br. J. Med. Psychol. 1974 47 211 218
40. W. T. Friedewald R. I. Levy D. S. Fredrickson Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge Clin. Chem. 1972 18 499 502
41. C. Heiss P. Kleinbongard A. Dejam S. Perré H. Schroeter H. Sies M. Kelm Acute consumption of flavanol-rich cocoa and the reversal of endothelial dysfunction in smokers J. Am. Coll. Cardiol. 2005 46 1276 1283
42. T. Rassaf P. Kleinbongard M. Preik A. Dejam P. Gharini T. Lauer J. Erckenbrecht A. Duschin R. Schulz G. Heusch M. Feelisch M. Kelm Plasma nitrosothiols contribute to the systemic vasodilator effects of intravenously applied NO: experimental and clinical study on the fate of NO in human blood Circ. Res. 2002 91 470 477
43. J. O. Lundberg E. Weitzberg NO generation from nitrite and its role in vascular control Arterioscler., Thromb., Vasc. Biol. 2005 25 915 922
44. N. D. L. Fisher M. Hughes M. Gerhard-Herman N. K. Hollenberg Flavanol-rich cocoa induces nitric-oxide-dependent vasodilation in healthy humans J. Hypertens. 2003 21 2281 2286
45. C. G. Fraga M. Galleano S. V. Verstraeten P. I. Oteiza Basic biochemical mechanisms behind the health benefits of polyphenols Mol. Aspects Med. 2010 31 435 445
46. R. J. Gryglewski R. Korbut J. Robak On the mechanism of antithrombotic action of flavonoids Biochem. Pharmacol. 1987 36 317 322
47. P. Mladenka L. Zatloukalova T. Filipsky R. Hrdina Cardiovascular effects of flavonoids are not caused only by direct antioxidant activity Free Radical Biol. Med. 2010 49 963 975
48. R. J. Nijveldt E. van Nood D. E. C. van Hoorn P. G. Boelens K. van Norren P. A. M. van Leeuwen Flavonoids: a review of probable mechanisms of action and potential applications Am. J. Clin. Nutr. 2001 74 418 425
49. A. Rodriguez-Mateos C. Rendeiro T. Bergillos-Meca S. Tabatabaee T. W. George C. Heiss J. P. Spencer Intake and time dependence of blueberry flavonoid-induced improvements in vascular function: a randomized, controlled, double-blind, crossover intervention study with mechanistic insights into biological activity Am. J. Clin. Nutr. 2013 98 1179 1191
50. M. F. McCarty Scavenging of peroxynitrite-derived radicals by flavonoids may support endothelial NO synthase activity, contributing to the vascular protection associated with high fruit and vegetable intakes Med. Hypotheses 2008 70 170 181
51. J. C. Stoclet T. Chataigneau M. Ndiaye M. H. Oak J. El Bedoui M. Chataigneau V. B. Schini-Kerth Vascular protection by dietary polyphenols Eur. J. Pharmacol. 2004 500 299 313
52. D. O. Kennedy E. L. Wightman J. L. Reay G. Lietz E. J. Okello A. Wilde C. F. Haskell Effects of resveratrol on cerebral blood flow variables and cognitive performance in humans: a double-blind, placebo-controlled, crossover investigation Am. J. Clin. Nutr. 2010 91 1590 1597
53. S. T. Francis K. Head P. G. Morris I. A. Macdonald The effect of flavanol-rich cocoa on the fMRI response to a cognitive task in healthy young people J. Cardiovasc. Pharmacol. 2006 47 S215 S220
54. D. T. Field C. M. Williams L. T. Butler Consumption of cocoa flavanols results in an acute improvement in visual and cognitive functions Physiol. Behav. 2011 103 255 260
55. M. M. Metzger D. F. Vanata Acute soy isoflavone consumption does not impact visual-spatial or verbal memory among healthy young adults N. Am. J. Psychol. 2007 9 379 386
56. A. B. Scholey S. J. French P. J. Morris D. O. Kennedy A. L. Milne C. F. Haskell Consumption of cocoa flavanols results in acute improvements in mood and cognitive performance during sustained mental effort J. Psychopharmacol. 2009 24 1505 1514
57. D. J. Lamport L. Dye J. D. Wightman C. L. Lawton The effects of flavonoid and other polyphenol consumption on cognitive performance: a systematic research review of human experimental and epidemiological studies Nutrition and Aging 2012 1 5 25
58. E. Farkas M. C. de Wilde A. J. Kiliaan P. G. Luiten Chronic cerebral hypoperfusion-related neuropathologic changes and compromised cognitive status: window of treatment Drugs Today 2002 38 365 376
59. A. L. Macready O. B. Kennedy J. A. Ellis C. M. Williams J. P. E. Spencer L. T. Butler Flavonoids and cognitive function: a review of human randomized controlled trial studies and recommendations for future studies Genes Nutr. 2009 4 227 242
60. E. Kesse-Guyot L. o. Fezeu V. A. Andreeva M. Touvier A. Scalbert S. Hercberg P. Galan Total and specific polyphenol intakes in midlife are associated with cognitive function measured 13 years later J. Nutr. 2011 142 76 83
61. L. Letenneur C. c. Proust-Lima A. l. Le Gouge J.-F. o. Dartigues P. Barberger-Gateau Flavonoid intake and cognitive decline over a 10-year period Am. J. Epidemiol. 2007 165 1364 1371
62. A. S. Pannala A. R. Mani J. P. Spencer V. Skinner K. R. Bruckdorfer K. P. Moore C. A. Rice-Evans The effect of dietary nitrate on salivary, plasma, and urinary nitrate metabolism in humans Free Radical Biol. Med. 2003 34 576 584
63. K. Cosby K. S. Partovi J. H. Crawford R. P. Patel C. D. Reiter S. Martyr B. K. Yang M. A. Waclawiw G. Zalos X. Xu K. T. Huang H. Shields D. B. Kim-Shapiro A. N. Schechter R. O. Cannon M. T. Gladwin Nitrite reduction to nitric oxide by deoxyhemoglobin vasodilates the human circulation Nat. Med. 2003 9 1498 1505
64. J. O. Lundberg E. Weitzberg M. T. Gladwin The nitrate-nitrite-nitric oxide pathway in physiology and therapeutics Nat. Rev. Drug Discovery 2008 7 156 167
65. T. D. Presley A. R. Morgan E. Bechtold W. Clodfelter R. W. Dove J. M. Jennings R. A. Kraft S. Bruce King P. J. Laurienti W. Jack Rejeski Acute effect of a high nitrate diet on brain perfusion in older adults Nitric Oxide 2011 24 34 42
66. J. Kelly J. Fulford A. Vanhatalo J. R. Blackwell O. French S. J. Bailey M. Gilchrist P. G. Winyard A. M. Jones Effects of short-term dietary nitrate supplementation on blood pressure, O2 uptake kinetics, and muscle and cognitive function in older adults Am. J. Physiol.: Regul., Integr. Comp. Physiol. 2013 304 R73 R83
67. E. Nurk H. Refsum C. A. Drevon G. S. Tell H. A. Nygaard K. Engedal A. D. Smith Cognitive performance among the elderly in relation to the intake of plant foods. The Hordaland Health Study Br. J. Nutr. 2010 104 1190
68. U. Takahama T. Oniki S. Hirota U. Takahama T. Oniki S. Hirota Oxidation of quercetin by salivary components. Quercetin-dependent reduction of salivary nitrite under acidic conditions producing nitric oxide J. Agric. Food Chem. 2002 50 4317 4322
69. U. Takahama M. Tanaka S. Hirota Proanthocyanidins in buckwheat flour can reduce salivary nitrite to nitric oxide in the stomach Plant Foods Hum. Nutr. 2010 65 1 7
70. J. Volk S. Gorelik R. Granit R. Kohen J. Kanner The dual function of nitrite under stomach conditions is modulated by reducing compounds Free Radical Biol. Med. 2009 47 496 502
71. B. S. Rocha B. Gago R. M. Barbosa J. Laranjinha Dietary polyphenols generate nitric oxide from nitrite in the stomach and induce smooth muscle relaxation Toxicology 2009 265 41 48
72. M. P. Pase A. B. Scholey A. Pipingas M. Kras K. Nolidin A. Gibbs K. Wesnes C. Stough Cocoa polyphenols enhance positive mood states but not cognitive performance: a randomized, placebo-controlled trial J. Psychopharmacol. 2013 27 451 458
73. A. Scholey L. A. Downey J. Ciorciari A. Pipingas K. Nolidin M. Finn M. Wines S. Catchlove A. Terrens E. Barlow L. Gordon C. Stough Acute neurocognitive effects of epigallocatechin gallate (EGCG) Appetite 2012 58 767 770