Pomegranate juice, but not an extract, confers a lower glycemic response on a high–glycemic index food: Randomized, crossover, controlled trials in healthy subjects

American Journal of Clinical Nutrition

Volumn 106, Issue 6, 2017, Pages 1384-1393

  Kerimi, Asimina ^a   Nyambe Silavwe, Hilda ^a   Gauer, Julia S ^a   Tomás Barberán, Francisco A ^b   Williamson, Gary ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

^b RESEARCH GROUP ON QUALITY   (Spain)

Author keywords

Carbohydrate digestion; Glucose transport; Glycemic index; Polyphenol; Starch

Indexed keywords

ACARBOSE; ALPHA GLUCOSIDASE; AMYLASE; AMYLASE INHIBITOR; CITRIC ACID; ELLAGIC ACID; FRUCTOSE; GLUCOSE; GLUCOSE TRANSPORTER 2; MALIC ACID; POLYPHENOL DERIVATIVE; POMEGRANATE EXTRACT; PUNICALAGIN; PUNICALIN; SUCRASE; UNCLASSIFIED DRUG; ANTIDIABETIC AGENT; PLANT MEDICINAL PRODUCT; POLYPHENOL; SLC2A2 PROTEIN, HUMAN; TANNIN;

ADULT; AGED; ANIMAL CELL; ARTICLE; BREAD; CACO-2 CELL LINE; COMPARATIVE EFFECTIVENESS; COMPETITIVE INHIBITION; CONTROLLED STUDY; CROSSOVER PROCEDURE; DOUBLE BLIND PROCEDURE; DRUG MEGADOSE; ENZYME INHIBITION ASSAY; GLUCOSE BLOOD LEVEL; GLUCOSE METABOLISM; GLUCOSE TRANSPORT; GLYCEMIC CONTROL; GLYCEMIC INDEX; HEP-G2 CELL LINE; HUMAN; HUMAN CELL; IC50; IN VITRO STUDY; INTESTINE BRUSH BORDER; INTESTINE FLORA; LOW DRUG DOSE; NONHUMAN; NORMAL HUMAN; OOCYTE; POMEGRANATE JUICE; RANDOMIZED CONTROLLED TRIAL; SUGAR TRANSPORT; TEST MEAL; XENOPUS; ANIMAL; AREA UNDER THE CURVE; CHEMISTRY; DRUG EFFECTS; FRUIT; FRUIT AND VEGETABLE JUICE; GLYCEMIC LOAD; LYTHRACEAE; METABOLISM; POSTPRANDIAL STATE; YOUNG ADULT;

ADULT; ANIMALS; AREA UNDER CURVE; BLOOD GLUCOSE; BREAD; CACO-2 CELLS; CROSS-OVER STUDIES; DOUBLE-BLIND METHOD; FRUIT; FRUIT AND VEGETABLE JUICES; GASTROINTESTINAL MICROBIOME; GLUCOSE TRANSPORTER TYPE 2; GLYCEMIC INDEX; GLYCEMIC LOAD; HEP G2 CELLS; HUMANS; HYDROLYZABLE TANNINS; HYPOGLYCEMIC AGENTS; PLANT PREPARATIONS; POLYPHENOLS; POSTPRANDIAL PERIOD; PUNICACEAE; YOUNG ADULT;

EID: 85038129992     PISSN: 00029165     EISSN: 19383207     Source Type: Journal    
DOI: 10.3945/ajcn.117.161968     Document Type: Article

References (36)

1. Russell WR, Baka A, Bjorck I, Delzenne N, Gao D, Griffiths HR, Hadjilucas E, Juvonen K, Lahtinen S, Lansink M, et al. Impact of diet composition on blood glucose regulation. Crit Rev Food Sci Nutr 2016; 56:541–90.
2. Livesey G, Taylor R, Hulshof T, Howlett J. Glycemic response and health–a systematic review and meta-analysis: relations between dietary glycemic properties and health outcomes. Am J Clin Nutr 2008; 87:258S–68S.
3. Blaak EE, Antoine JM, Benton D, Bjorck I, Bozzetto L, Brouns F, Diamant M, Dye L, Hulshof T, Holst JJ, et al. Impact of postprandial glycaemia on health and prevention of disease. Obes Rev 2012;13:923–84.
4. Asgary S, Sahebkar A, Afshani MR, Keshvari M, Haghjooyjavanmard S, Rafieian-Kopaei M. Clinical evaluation of blood pressure lowering, en-dothelial function improving, hypolipidemic and anti-inflammatory effects of pomegranate juice in hypertensive subjects. Phytother Res 2014; 28:193–9.
5. Lynn A, Hamadeh H, Leung WC, Russell JM, Barker ME. Effects of pomegranate juice supplementation on pulse wave velocity and blood pressure in healthy young and middle-aged men and women. Plant Foods Hum Nutr 2012;67:309–14.
6. Tsang C, Smail NF, Almoosawi S, Davidson I, Al-Dujaili EA. Intake of polyphenol-rich pomegranate pure juice influences urinary glucocor-ticoids, blood pressure and homeostasis model assessment of insulin resistance in human volunteers. J Nutr Sci 2012;1:e9.
7. González-Ortiz M, Martínez-Abundis E, Espinel-Bermúdez MC, Pérez-Rubio KG. Effect of pomegranate juice on insulin secretion and sensitivity in patients with obesity. Ann Nutr Metab 2011;58:220–3.
8. Aviram M, Dornfeld L. Pomegranate juice consumption inhibits serum angiotensin converting enzyme activity and reduces systolic blood pressure. Atherosclerosis 2001;158:195–8.
9. Kam A, Li KM, Razmovski-Naumovski V, Nammi S, Shi J, Chan K, Li GQ. A comparative study on the inhibitory effects of different parts and chemical constituents of pomegranate on alpha-amylase and alpha-glucosidase. Phytother Res 2013;27:1614–20.
10. Bellesia A, Verzelloni E, Tagliazucchi D. Pomegranate ellagitannins inhibit alpha-glucosidase activity in vitro and reduce starch digestibility under simulated gastro-intestinal conditions. Int J Food Sci Nutr 2015;66:85–92.
11. Barrett A, Ndou T, Hughey CA, Straut C, Howell A, Dai Z, Kaletunc G. Inhibition of alpha-amylase and glucoamylase by tannins extracted from cocoa, pomegranates, cranberries, and grapes. J Agric Food Chem 2013;61:1477–86.
12. Cerdá B, Cerón JJ, Tomás-Barberán FA, Espín JC. Repeated oral administration of high doses of the pomegranate ellagitannin punicalagin to rats for 37 days is not toxic. J Agric Food Chem 2003;51:3493–501.
13. González-Sarrías A, García-Villalba R, Romo-Vaquero M, Alasalvar C, Örem A, Zafrilla P, Tomás-Barberán FA, Selma MV, Espín JC. Clustering according to urolithin metabotype explains the interindividual variability in the improvement of cardiovascular risk biomarkers in overweight-obese individuals consuming pomegranate: A randomized clinical trial. Mol Nutr Food Res 2017;61.
14. Garía-Villalba R, Espín JC, Tomás-Barberán FA. Chromatographic and spectroscopic characterization of urolithins for their determination in biological samples after the intake of foods containing ellagitannins and ellagic acid. J Chromatogr A 2016;1428:162–75.
15. García-Villalba R, Espín JC, Aaby K, Alasalvar C, Heinonen M, Jacobs G, Voorspoels S, Koivumäki T, Kroon PA, Pelvan E, et al. Validated method for the characterization and quantification of extractable and nonextractable ellagitannins after acid hydrolysis in pomegranate fruits, juices, and extracts. J Agric Food Chem 2015;63:6555–66.
16. Ifie I, Marshall LJ, Ho P, Williamson G. Hibiscus sabdariffa (Roselle) extracts and wine: phytochemical profile, physicochemical properties, and carbohydrase inhibition. J Agric Food Chem 2016;64:4921–31.
17. Krueger DA. Composition of pomegranate juice. J AOAC Int 2012;95: 163–8.
18. Englyst HN, Kingman SM, Cummings JH. Classification and measurement of nutritionally important starch fractions. Eur J Clin Nutr 1992;46:S33–50.
19. Nyambe-Silavwe H, Williamson G. Polyphenol- and fibre-rich dried fruits with green tea attenuate starch-derived postprandial blood glucose and insulin: a randomised, controlled, single-blind, cross-over intervention. Br J Nutr 2016;116:443–50.
20. Nyambe-Silavwe H, Villa-Rodriguez JA, Ifie I, Holmes M, Aydin E, Jensen JM, Williamson G. Inhibition of human alpha-amylase by dietary polyphenols. J Funct Foods 2015;19:723–32.
21. Kerimi A, Jailani F, Williamson G. Modulation of cellular glucose metabolism in human HepG2 cells by combinations of structurally related flavonoids. Mol Nutr Food Res 2015;59:894–906.
22. Villa-Rodriguez JA, Aydin E, Gauer JS, Pyner A, Williamson G, Kerimi A. Green and chamomile teas, but not acarbose, attenuate glucose and fructose transport via inhibition of GLUT2 and GLUT5. Mol Nutr Food Res 2017 Sep 3 (Epub ahead of print; DOI: 10.1002/ mnfr.201700566).
23. Sun D, Lennernas H, Welage LS, Barnett JL, Landowski CP, Foster D, Fleisher D, Lee KD, Amidon GL. Comparison of human duodenum and Caco-2 gene expression profiles for 12,000 gene sequences tags and correlation with permeability of 26 drugs. Pharm Res 2002;19:1400–16.
24. Manzano S, Williamson G. Polyphenols and phenolic acids from strawberry and apple decrease glucose uptake and transport by human intestinal Caco-2 cells. Mol Nutr Food Res 2010;54:1773–80.
25. Johnston CS, Steplewska I, Long CA, Harris LN, Ryals RH. Examination of the antiglycemic properties of vinegar in healthy adults. Ann Nutr Metab 2010;56:74–9.
26. Wills RBH, Miller JCB, Matawie KM. Relationship between glycae-mic index and nutrient composition of fruit and vegetables. Int J Food Prop 1998;1:89–94.
27. Liljeberg HGM, Lonner CH, Bjorck IME. Sourdough fermentation or addition of organic-acids or corresponding salts to bread improves nutritional properties of starch in healthy humans. J Nutr 1995;125:1503–11.
28. Taylor RH, Jenkins DJ, Barker HM, Fielden H, Goff DV, Misiewicz JJ, Lee DA, Allen HB, MacDonald G, Wallrabe H. Effect of acarbose on the 24-hour blood glucose profile and pattern of carbohydrate absorption. Diabetes Care 1982;5:92–6.
29. Hanefeld M, Schaper F, Koehler C. Effect of acarbose on vascular disease in patients with abnormal glucose tolerance. Cardiovasc Drugs Ther 2008;22:225–31.
30. Chiasson JL, Josse RG, Gomis R, Hanefeld M, Karasik A, Laakso M. Acarbose treatment and the risk of cardiovascular disease and hypertension in patients with impaired glucose tolerance: the STOP-NIDDM trial. JAMA 2003;290:486–94.
31. Banihani SA, Makahleh SM, El-Akawi Z, Al-Fashtaki RA, Khabour OF, Gharibeh MY, Saadah NA, Al-Hashimi FH, Al-Khasieb NJ. Fresh pomegranate juice ameliorates insulin resistance, enhances beta-cell function, and decreases fasting serum glucose in type 2 diabetic patients. Nutr Res 2014;34:862–7.
32. Fuster-Muñoz E, Roche E, Funes L, Martínez-Peinado P, Sempere JM, Vicente-Salar N. Effects of pomegranate juice in circulating parameters, cytokines, and oxidative stress markers in endurance-based athletes: A randomized controlled trial. Nutrition 2016;32:539–45.
33. Sohrab G, Angoorani P, Tohidi M, Tabibi H, Kimiagar M, Nasrollahzadeh J. Pomegranate (Punicagranatum) juice decreases lipid peroxidation, but has no effect on plasma advanced glycated end-products in adults with type 2 diabetes: a randomized double-blind clinical trial. Food Nutr Res 2015;59:28551.
34. Kim DH, Kwack SJ, Yoon KS, Choi JS, Lee BM. 4-Hydroxynonenal: a superior oxidative biomarker compared to malondialdehyde and carbonyl content induced by carbon tetrachloride in rats. J Toxicol Environ Health A 2015;78:1051–62.
35. Seeram NP, Zhang Y, McKeever R, Henning SM, Lee RP, Suchard MA, Li Z, Chen S, Thames G, Zerlin A, et al. Pomegranate juice and extracts provide similar levels of plasma and urinary ellagitannin metabolites in human subjects. J Med Food 2008;11: 390–4.
36. Romo-Vaquero M, Garcia-Villalba R, Gonzalez-Sarrias A, Beltran D, Tomas-Barberan FA, Espin JC, Selma MV. Interindividual variability in the human metabolism of ellagic acid: contribution of Gordoni-bacter to urolithin production. J Funct Foods 2015;17:785–91.