Interindividual variability in biomarkers of cardiometabolic health after consumption of major plant-food bioactive compounds and the determinants involved

Advances in Nutrition

Volumn 8, Issue 4, 2017, Pages 558-570

  Milenkovic, Dragan ^a   Morand, Christine ^a   Cassidy, Aedin ^b   Konic Ristic, Aleksandra ^c   Tomás Barberán, Francisco ^d   Ordovas, José M ^e,f   Kroon, Paul ^g   Caterina, Raffaele De ^h   Rodriguez Mateos, Ana ⁱ  

^a INRA and University of Auvergne   (France)

^b UNIVERSITY OF EAST ANGLIA   (United Kingdom)

^c UNIVERSITY OF LEEDS   (United Kingdom)

^d RESEARCH GROUP ON QUALITY   (Spain)

^e TUFTS UNIVERSITY   (United States)

^f IMDEA FOOD INSTITUTE   (Spain)

^g NORWICH RESEARCH PARK   (United Kingdom)

^h INSTITUTE OF CLINICAL PHYSIOLOGY   (Italy)

ⁱ HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

Biological responsiveness; Cardiometabolic health; Determinants of interindividual variability; Interindividual variability; Plant food bioactives

Indexed keywords

BIOLOGICAL MARKER; PHYTOCHEMICAL; POLYPHENOL;

BLOOD; CARDIOVASCULAR DISEASE; FEMALE; GENETIC POLYMORPHISM; HUMAN; MALE; METABOLIC SYNDROME X; NON INSULIN DEPENDENT DIABETES MELLITUS; OBESITY; RANDOMIZED CONTROLLED TRIAL (TOPIC); RISK FACTOR; SEX FACTOR;

BIOMARKERS; CARDIOVASCULAR DISEASES; DIABETES MELLITUS, TYPE 2; FEMALE; HUMANS; MALE; METABOLIC SYNDROME; OBESITY; PHYTOCHEMICALS; POLYMORPHISM, GENETIC; POLYPHENOLS; RANDOMIZED CONTROLLED TRIALS AS TOPIC; RISK FACTORS; SEX FACTORS;

EID: 85024406463     PISSN: 21618313     EISSN: 21565376     Source Type: Journal    
DOI: 10.3945/an.116.013623     Document Type: Review

References (85)

1. Castro JP, El-Atat FA, McFarlane SI, Aneja A, Sowers JR. Cardiometabolic syndrome: pathophysiology and treatment. Curr Hypertens Rep 2003;5:393-401
2. Ezzati M, Riboli E. Behavioral and dietary risk factors for noncommunicable diseases. N Engl J Med 2013;369:954-64
3. Holst B, Williamson G. Nutrients and phytochemicals: from bioavailability to bioefficacy beyond antioxidants. Curr Opin Biotechnol 2008; 19:73-82
4. Manach C, Scalbert A, Morand C, Remesy C, Jimenez L. Polyphenols: food sources and bioavailability. Am J Clin Nutr 2004;79:727-47
5. Khoo HE, Prasad KN, Kong KW, Jiang Y, Ismail A. Carotenoids and their isomers: color pigments in fruits and vegetables. Molecules 2011; 16:1710-38
6. Ostlund RE Jr. Phytosterols in human nutrition. Annu Rev Nutr 2002; 22:533-49
7. Heckman MA, Weil J, Gonzalez de Mejia E. Caffeine (1, 3, 7-trimethylxanthine) in foods: a comprehensive review on consumption, functionality, safety, and regulatory matters. J Food Sci 2010;75:R77-87
8. Wang X, Ouyang Y, Liu J, Zhu M, Zhao G, Bao W, Hu FB. Fruit and vegetable consumption and mortality from all causes, cardiovascular disease, and cancer: systematic review and dose-response meta-analysis of prospective cohort studies. BMJ 2014;349:g4490
9. Auclair S, Milenkovic D, Besson C, Chauvet S, Gueux E, Morand C, Mazur A, Scalbert A. Catechin reduces atherosclerotic lesion development in apo E-deficient mice: a transcriptomic study. Atherosclerosis 2009;204:e21-7
10. Chanet A, Milenkovic D, Deval C, Potier M, Constans J, Mazur A, Bennetau-Pelissero C, Morand C, Berard AM. Naringin, the major grapefruit flavonoid, specifically affects atherosclerosis development in diet-induced hypercholesterolemia in mice. J Nutr Biochem 2012;23:469-77
11. Del Rio D, Rodriguez-Mateos A, Spencer JP, Tognolini M, Borges G, Crozier A. Dietary (poly)phenolics in human health: structures, bioavailability, and evidence of protective effects against chronic diseases. Antioxid Redox Signal 2013;18:1818-92
12. Habauzit V, Morand C. Evidence for a protective effect of polyphenolscontaining foods on cardiovascular health: an update for clinicians. Ther Adv Chronic Dis 2012;3:87-106
13. Hooper L, Kay C, Abdelhamid A, Kroon PA, Cohn JS, Rimm EB, Cassidy A. Effects of chocolate, cocoa, and flavan-3-ols on cardiovascular health: a systematic review and meta-analysis of randomized trials. Am J Clin Nutr 2012;95:740-51
14. Hooper L, Kroon PA, Rimm EB, Cohn JS, Harvey I, Le Cornu KA, Ryder JJ, Hall WL, Cassidy A. Flavonoids, flavonoid-rich foods, and cardiovascular risk: a meta-analysis of randomized controlled trials. Am J Clin Nutr 2008;88:38-50
15. AbuMweis SS, Marinangeli CP, Frohlich J, Jones PJ. Implementing phytosterols into medical practice as a cholesterol-lowering strategy: overview of efficacy, effectiveness, and safety. Can J Cardiol 2014;30:1225-32
16. O'Keefe JH, Bhatti SK, Patil HR, DiNicolantonio JJ, Lucan SC, Lavie CJ. Effects of habitual coffee consumption on cardiometabolic disease, cardiovascular health, and all-cause mortality. J Am Coll Cardiol 2013;62:1043-51
17. Wu JN, Ho SC, Zhou C, Ling WH, Chen WQ, Wang CL, Chen YM. Coffee consumption and risk of coronary heart diseases: a meta-analysis of 21 prospective cohort studies. Int J Cardiol 2009;137:216-25
18. Rodriguez-Mateos A, Vauzour D, Krueger CG, Shanmuganayagam D, Reed J, Calani L, Mena P, Del Rio D, Crozier A. Bioavailability, bioactivity and impact on health of dietary flavonoids and related compounds: an update. Arch Toxicol 2014;88:1803-53
19. CornelisMC, El-Sohemy A, Kabagambe EK, Campos H. Coffee, CYP1A2 genotype, and risk of myocardial infarction. JAMA 2006;295:1135-41
20. Guadamuro L, Delgado S, Redruello B, Florez AB, Suarez A, Martinez-Camblor P, Mayo B. Equol status and changes in fecal microbiota in menopausal women receiving long-term treatment for menopause symptoms with a soy-isoflavone concentrate. Front Microbiol 2015;6:777
21. Setchell KD, Cole SJ. Method of defining equol-producer status and its frequency among vegetarians. J Nutr 2006;136:2188-93
22. Setchell KD, Clerici C. Equol: history, chemistry, and formation. J Nutr 2010;140:1355S-62S
23. Espin JC, Larrosa M, Garcia-Conesa MT, Tomas-Barberan F. Biological significance of urolithins, the gut microbial ellagic Acid-derived metabolites: the evidence so far. Evid Based Complement Alternat Med 2013;2013:270418
24. Landete JM. Updated knowledge about polyphenols: functions, bioavailability, metabolism, and health. Crit Rev Food Sci Nutr 2012;52: 936-48. Retraction of: Crit Rev Food Sci Nutr. 2015;55:1792
25. Sachse C, Brockmoller J, Bauer S, Roots I. Functional significance of a C/A polymorphism in intron 1 of the cytochrome P450 CYP1A2-gene tested with caffeine. Br J Clin Pharmacol 1999;47:445-9
26. Dellinger RW, Garcia AM, Meyskens FL Jr. Differences in the glucuronidation of resveratrol and pterostilbene: altered enzyme specificity and potential gender differences. Drug Metab Pharmacokinet 2014;29:112-9
27. Manach C, Milenkovic D, Van de Wiele T, Rodriguez-Mateos A, de Roos B, Garcia-Conesa MT, Landberg R, Gibney ER, Heinonen M, Tomas-Barberan F, et al. Addressing the inter-individual variation in response to consumption of plant food bioactives-towards a better understanding of their role in healthy ageing and cardiometabolic risk reduction. Mol Nutr Food Res 2016 Sep 30 (Epub ahead of print; DOI: 10.1002/mnfr.201600557)
28. Franklin SS, Jacobs MJ, Wong ND, L'Italien GJ, Lapuerta P. Predominance of isolated systolic hypertension among middle-aged and elderly US hypertensives: analysis based on National Health and Nutrition Examination Survey (NHANES) III. Hypertension 2001;37:869-74
29. Wilson PW, D'Agostino RB, Levy D, Belanger AM, Silbershatz H, Kannel WB. Prediction of coronary heart disease using risk factor categories. Circulation 1998;97:1837-47
30. Egert S, Bosy-Westphal A, Seiberl J, Kurbitz C, Settler U, Plachta-Danielzik S, Wagner AE, Frank J, Schrezenmeir J, Rimbach G, et al. Quercetin reduces systolic blood pressure and plasma oxidised low-density lipoprotein concentrations in overweight subjects with a high-cardiovascular disease risk phenotype: a doubleblinded, placebo-controlled cross-over study. Br J Nutr 2009;102: 1065-74
31. Avolio AP, Deng FQ, Li WQ, Luo YF, Huang ZD, Xing LF, O'Rourke MF. Effects of aging on arterial distensibility in populations with high and low prevalence of hypertension: comparison between urban and rural communities in China. Circulation 1985; 71:202-10
32. McLean AJ, Le Couteur DG. Aging biology and geriatric clinical pharmacology. Pharmacol Rev 2004;56:163-84
33. Thijssen DH, Black MA, Pyke KE, Padilla J, Atkinson G, Harris RA, Parker B, Widlansky ME, Tschakovsky ME, Green DJ. Assessment of flow-mediated dilation in humans: a methodological and physiological guideline. Am J Physiol Heart Circ Physiol 2011;300:H2-12
34. Fisher ND, Hollenberg NK. Aging and vascular responses to flavanolrich cocoa. J Hypertens 2006;24:1575-80
35. Mubarak A, Bondonno CP, Liu AH, Considine MJ, Rich L, Mas E, Croft KD, Hodgson JM. Acute effects of chlorogenic acid on nitric oxide status, endothelial function, and blood pressure in healthy volunteers: a randomized trial. J Agric Food Chem 2012;60:9130-6
36. Mackay DS, Gebauer SK, Eck PK, Baer DJ, Jones PJ. Lathosterol-tocholesterol ratio in serum predicts cholesterol-lowering response to plant sterol consumption in a dual-center, randomized, single-blind placebo-controlled trial. Am J Clin Nutr 2015;101:432-9
37. Nagao T, Meguro S, Hase T, Otsuka K, Komikado M, Tokimitsu I, Yamamoto T, Yamamoto K. A catechin-rich beverage improves obesity and blood glucose control in patients with type 2 diabetes. Obesity (Silver Spring) 2009;17:310-7
38. Rodriguez-Mateos A, Cifuentes-Gomez T, Gonzalez-Salvador I, Ottaviani JI, Schroeter H, Kelm M, Heiss C, Spencer JP. Influence of age on the absorption, metabolism, and excretion of cocoa flavanols in healthy subjects. Mol Nutr Food Res 2015;59:1504-12
39. Weber T, Auer J, O'Rourke MF, Kvas E, Lassnig E, Berent R, Eber B. Arterial stiffness, wave reflections, and the risk of coronary artery disease. Circulation 2004;109:184-9
40. Corretti MC, Anderson TJ, Benjamin EJ, Celermajer D, Charbonneau F, Creager MA, Deanfield J, Drexler H, Gerhard-Herman M, Herrington D, et al. Guidelines for the ultrasound assessment of endothelial-dependent flow-mediated vasodilation of the brachial artery: a report of the International Brachial Artery Reactivity Task Force. J Am Coll Cardiol 2002;39:257-65
41. Hollman PC, Cassidy A, Comte B, Heinonen M, Richelle M, Richling E, Serafini M, Scalbert A, Sies H, Vidry S. The biological relevance of direct antioxidant effects of polyphenols for cardiovascular health in humans is not established. J Nutr 2011;141:989S-1009S
42. Ostertag LM, Kroon PA, Wood S, Horgan GW, Cienfuegos-Jovellanos E, Saha S, Duthie GG, de Roos B. Flavan-3-ol-enriched dark chocolate and white chocolate improve acute measures of platelet function in a gender-specific way-a randomized-controlled human intervention trial. Mol Nutr Food Res 2013;57:191-202
43. West SG, McIntyre MD, Piotrowski MJ, Poupin N, Miller DL, Preston AG, Wagner P, Groves LF, Skulas-Ray AC. Effects of dark chocolate and cocoa consumption on endothelial function and arterial stiffness in overweight adults. Br J Nutr 2014;111:653-61
44. Kaya A, Uzunhasan I, Baskurt M, Ozkan A, Ataoglu E, Okcun B, Yigit Z. Oxidative status and lipid profile in metabolic syndrome: gender differences. Metab Syndr Relat Disord 2010;8:53-8
45. Ibero-Baraibar I, Abete I, Navas-Carretero S, Massis-Zaid A, Martinez JA, Zulet MA. Oxidised LDL levels decreases after the consumption of ready-to-eat meals supplemented with cocoa extract within a hypocaloric diet. Nutrition, metabolism, and cardiovascular diseases. Nutr Metab Cardiovasc Dis 2014;24:416-22
46. Cai Y, Guo K, Chen C, Wang P, Zhang B, Zhou Q, Mei F, Su Y. Soya isoflavone consumption in relation to carotid intima-media thickness in Chinese equol excretors aged 40-65 years. Br J Nutr 2012;108:1698-704
47. Setchell KD, Cassidy A. Dietary isoflavones: biological effects and relevance to human health. J Nutr 1999;129:758S-67S
48. Kreijkamp-Kaspers S, Kok L, Bots ML, Grobbee DE, van der Schouw YT. Dietary phytoestrogens and vascular function in postmenopausal women: a cross-sectional study. J Hypertens 2004;22:1381-8
49. Happonen P, Voutilainen S, Tuomainen TP, Salonen JT. Catechol-omethyltransferase gene polymorphism modifies the effect of coffee intake on incidence of acute coronary events. PLoS One 2006;1:e117
50. Palatini P, Ceolotto G, Ragazzo F, Dorigatti F, Saladini F, Papparella I, Mos L, Zanata G, Santonastaso M. CYP1A2 genotype modifies the association between coffee intake and the risk of hypertension. J Hypertens 2009;27:1594-601
51. Palatini P, Benetti E, Mos L, Garavelli G, Mazzer A, Cozzio S, Fania C, Casiglia E. Association of coffee consumption and CYP1A2 polymorphism with risk of impaired fasting glucose in hypertensive patients. Eur J Epidemiol 2015;30:209-17
52. Fox GP, Wu A, Yiran L, Force L. Variation in caffeine concentration in single coffee beans. J Agric Food Chem 2013;61:10772-8
53. Conroy RM, Pyorala K, Fitzgerald AP, Sans S, Menotti A, De Backer G, De Bacquer D, Ducimetiere P, Jousilahti P, Keil U, et al. Estimation of ten-year risk of fatal cardiovascular disease in Europe: the SCORE project. Eur Heart J 2003;24:987-1003
54. Celermajer DS, Sorensen KE, Spiegelhalter DJ, Georgakopoulos D, Robinson J, Deanfield JE. Aging is associated with endothelial dysfunction in healthy men years before the age-related decline in women. J Am Coll Cardiol 1994;24:471-6
55. Fisher G, Brown AW, Bohan Brown MM, Alcorn A, Noles C, Winwood L, Resuehr H, George B, Jeansonne MM, Allison DB. High intensity interval-vs moderate intensity-training for improving cardiometabolic health in overweight or obese males: a randomized controlled trial. PLoS One 2015;10:e0138853
56. Heiss C, Sansone R, Karimi H, Krabbe M, Schuler D, Rodriguez-Mateos A, Kraemer T, Cortese-Krott MM, Kuhnle GG, Spencer JP, et al. Impact of cocoa flavanol intake on age-dependent vascular stiffness in healthy men: a randomized, controlled, double-masked trial. Age (Dordr) 2015;37:9794
57. Miller RJ, Jackson KG, Dadd T, Mayes AE, Brown AL, Lovegrove JA, Minihane AM. The impact of the catechol-O-methyltransferase genotype on vascular function and blood pressure after acute green tea ingestion. Mol Nutr Food Res 2012;56:966-75
58. Miller RJ, Jackson KG, Dadd T, Mayes AE, Brown AL, Minihane AM. The impact of the catechol-O-methyltransferase genotype on the acute responsiveness of vascular reactivity to a green tea extract. Br J Nutr 2011;105:1138-44
59. Renda G, Zimarino M, Antonucci I, Tatasciore A, Ruggieri B, Bucciarelli T, Prontera T, Stuppia L, De Caterina R. Genetic determinants of blood pressure responses to caffeine drinking. Am J Clin Nutr 2012;95:241-8
60. Strandhagen E, Zetterberg H, Aires N, Palmer M, Rymo L, Blennow K, Landaas S, Thelle DS. The methylenetetrahydrofolate reductase C677T polymorphism is a major determinant of coffee-induced increase of plasma homocysteine: a randomized placebo controlled study. Int J Mol Med 2004;13:811-5
61. Strandhagen E, Zetterberg H, Aires N, Palmer M, Rymo L, Blennow K, Thelle DS. The apolipoprotein E polymorphism and the cholesterolraising effect of coffee. Lipids Health Dis 2004;3:26
62. De Castro-Orós I, Pampín S, Cofán M, Mozas P, Pintó X, Salas-Salvadó J, Rodríguez-Rey JC, Ros E, Civeira F, Pocoví M. Promoter variant-204A>C of the cholesterol 7alpha-hydroxylase gene: association with response to plant sterols in humans and increased transcriptional activity in transfected HepG2 cells. Clin Nutr 2011;30:239-46
63. Sanchez-Muniz FJ, Maki KC, Schaefer EJ, Ordovas JM. Serum lipid and antioxidant responses in hypercholesterolemic men and women receiving plant sterol esters vary by apolipoprotein E genotype. J Nutr 2009;139:13-9
64. Zhao HL, Houweling AH, Vanstone CA, Jew S, Trautwein EA, Duchateau GS, Jones PJ. Genetic variation in ABC G5/G8 and NPC1L1 impact cholesterol response to plant sterols in hypercholesterolemic men. Lipids 2008;43:1155-64
65. Rideout TC, Harding SV, Mackay D, Abumweis SS, Jones PJ. High basal fractional cholesterol synthesis is associated with nonresponse of plasma LDL cholesterol to plant sterol therapy. Am J Clin Nutr 2010;92:41-6
66. Welty FK, Lee KS, Lew NS, Zhou JR. Effect of soy nuts on blood pressure and lipid levels in hypertensive, prehypertensive, and normotensive postmenopausal women. Arch Intern Med 2007;167:1060-7
67. Heiss C, Finis D, Kleinbongard P, Hoffmann A, Rassaf T, KelmM, Sies H. Sustained increase in flow-mediated dilation after daily intake of highflavanol cocoa drink over 1 week. J Cardiovasc Pharmacol 2007;49:74-80
68. Morand C, Dubray C, Milenkovic D, Lioger D, Martin JF, Scalbert A, Mazur A. Hesperidin contributes to the vascular protective effects of orange juice: a randomized crossover study in healthy volunteers. Am J Clin Nutr 2011;93:73-80
69. Rodriguez-Mateos A, Rendeiro C, Bergillos-Meca T, Tabatabaee S, George TW, Heiss C, Spencer JP. 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;98:1179-91
70. Schroeter H, Heiss C, Balzer J, Kleinbongard P, Keen CL, Hollenberg NK, Sies H, Kwik-Uribe C, Schmitz HH, Kelm M. (-)-Epicatechin mediates beneficial effects of flavanol-rich cocoa on vascular function in humans. Proc Natl Acad Sci USA 2006;103:1024-9
71. Selma MV, Espin JC, Tomas-Barberan FA. Interaction between phenolics and gut microbiota: role in human health. J Agric Food Chem 2009;57:6485-501
72. Arumugam M, Raes J, Pelletier E, Le Paslier D, Yamada T, Mende DR, Fernandes GR, Tap J, Bruls T, Batto JM, et al. Enterotypes of the human gut microbiome. Nature 2011;473:174-80
73. Le Chatelier E, Nielsen T, Qin J, Prifti E, Hildebrand F, Falony G, Almeida M, ArumugamM, Batto JM, Kennedy S, et al. Richness of human gut microbiome correlates with metabolic markers. Nature 2013;500:541-6
74. Wong JM, Kendall CW, Marchie A, Liu Z, Vidgen E, Holmes C, Jackson CJ, Josse RG, Pencharz PB, Rao AV, et al. Equol status and blood lipid profile in hyperlipidemia after consumption of diets containing soy foods. Am J Clin Nutr 2012;95:564-71
75. Usui T, Tochiya M, Sasaki Y, Muranaka K, Yamakage H, Himeno A, Shimatsu A, Inaguma A, Ueno T, Uchiyama S, et al. Effects of natural S-equol supplements on overweight or obesity and metabolic syndrome in the Japanese, based on sex and equol status. Clin Endocrinol (Oxf) 2013;78:365-72
76. Hazim S, Curtis PJ, Schar MY, Ostertag LM, Kay CD, Minihane AM, Cassidy A. Acute benefits of the microbial-derived isoflavone metabolite equol on arterial stiffness in men prospectively recruited according to equol producer phenotype: a double-blind randomized controlled trial. Am J Clin Nutr 2016;103:694-702
77. Cho I, Yamanishi S, Cox L, Methe BA, Zavadil J, Li K, Gao Z, Mahana D, Raju K, Teitler I, et al. Antibiotics in early life alter the murine colonic microbiome and adiposity. Nature 2012;488:621-6
78. Qin J, Li Y, Cai Z, Li S, Zhu J, Zhang F, Liang S, Zhang W, Guan Y, Shen D, et al. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature 2012;490:55-60
79. Wang Z, Klipfell E, Bennett BJ, Koeth R, Levison BS, Dugar B, Feldstein AE, Britt EB, Fu X, Chung YM, et al. Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease. Nature 2011;472:57-63
80. Ridaura VK, Faith JJ, Rey FE, Cheng J, Duncan AE, Kau AL, Griffin NW, Lombard V, Henrissat B, Bain JR, et al. Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science 2013;341:1241214
81. Koeth RA, Wang Z, Levison BS, Buffa JA, Org E, Sheehy BT, Britt EB, Fu X, Wu Y, Li L, et al. Intestinal microbiota metabolism of L-carnitine, a nutrient in red meat, promotes atherosclerosis. Nat Med 2013;19:576-85
82. Clavel T, Desmarchelier C, Haller D, Gerard P, Rohn S, Lepage P, Daniel H. Intestinal microbiota in metabolic diseases: from bacterial community structure and functions to species of pathophysiological relevance. Gut Microbes 2014;5:544-51
83. Tomás-Barberán FA, García-Villalba R, González-Sarrías A, Selma MV, Espín JC. Ellagic acid metabolism by human gut microbiota: consistent observation of three urolithin phenotypes in intervention trials, independent of food source, age, and health status. J Agric Food Chem 2014;62:6535-8
84. Mora-Cubillos X, Tulipani S, Garcia-Aloy M, Bullo M, Tinahones FJ, Andres-Lacueva C. Plasma metabolomic biomarkers of mixed nuts exposure inversely correlate with severity of metabolic syndrome. Mol Nutr Food Res 2015;59:2480-90
85. Selma MV, Romo-Vaquero M, Garcia-Villalba R, Gonzalez-Sarrias A, Tomas-Barberan FA, Espin JC. The human gut microbial ecology associated with overweight and obesity determines ellagic acid metabolism. Food Funct 2016;7:1769-74