Plasma bioavailability and regional brain distribution of polyphenols from apple/grape seed and bilberry extracts in a young swine model

Molecular Nutrition and Food Research

Volumn 59, Issue 12, 2015, Pages 2432-2447

  Chen, Tzu Ying ^a   Kritchevsky, Janice ^b   Hargett, Katherine ^a   Feller, Kathryn ^a   Klobusnik, Ryan ^a   Song, Brian J ^c   Cooper, Bruce ^c   Jouni, Zeina ^d,e   Ferruzzi, Mario G ^a,c   Janle, Elsa M ^a  

^a PURDUE UNIVERSITY   (United States)

^b PURDUE UNIVERSITY   (United States)

^c PURDUE UNIVERSITY   (United States)

^d Mead Johnson Nutritionals   (United States)

^e KELLOGG COMPANY   (United States)

Author keywords

Anthocyanins; Brain distribution; Catechins; Pharmacokinetics; Polyphenols

Indexed keywords

ANTHOCYANIN; GRAPE SEED EXTRACT; PLANT EXTRACT; POLYPHENOL;

ANIMAL; BILBERRY; BIOAVAILABILITY; BLOOD; BODY WEIGHT; BRAIN; CHEMISTRY; DOSE RESPONSE; DRUG EFFECTS; EATING; ENZYMOLOGY; LIVER; MALUS; METABOLISM; PIG; TISSUE DISTRIBUTION; URINE; VITIS; WEANING;

ANIMALS; ANTHOCYANINS; BIOLOGICAL AVAILABILITY; BODY WEIGHT; BRAIN; DOSE-RESPONSE RELATIONSHIP, DRUG; EATING; GRAPE SEED EXTRACT; LIVER; MALUS; PLANT EXTRACTS; POLYPHENOLS; SUS SCROFA; TISSUE DISTRIBUTION; VACCINIUM MYRTILLUS; VITIS; WEANING;

EID: 84954365721     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.201500224     Document Type: Article

References (63)

1. Ebrahimi, A., Schluesener, H., Natural polyphenols against neurodegenerative disorders: potentials and pitfalls. Ageing Res. Rev. 2012, 11, 329-345.
2. Campos-Esparza Mdel, R., Torres-Ramos, M. A., Neuroprotection by natural polyphenols: molecular mechanisms. Cent. Nerv. Syst. Agents Med. Chem. 2010, 10, 269-277.
3. Albarracin, S. L., Stab, B., Casas, Z., Sutachan, J. J. et.al., Effects of natural antioxidants in neurodegenerative disease. Nutr. Neurosci. 2012, 15, 1-9.
4. Gu, L., Kelm, M. A., Hammerstone, J. F., Beecher, G. et al., Concentrations of proanthocyanidins in common foods and estimations of normal consumption. J. Nutr. 2004, 134, 613-617.
5. Johannot, L., Somerset, S. M., Age-related variations in flavonoid intake and sources in the Australian population. Public Health Nutr. 2006, 9, 1045-1054.
6. Drossard, C., Alexy, U., Bolzenius, K., Kunz, C. et al., Anthocyanins in the diet of infants and toddlers: intake, sources and trends. Eur. J. Nutr. 2011, 50, 705-711.
7. Vingtdeux, V., Giliberto, L., Zhao, H., Chandakkar, P. et al., AMP-activated protein kinase signaling activation by resveratrol modulates amyloid-beta peptide metabolism. J. Biol. Chem. 2010, 285, 9100-9113.
8. Wang, J., Ferruzzi, M. G., Ho, L., Blount, J. et al., Brain-targeted proanthocyanidin metabolites for Alzheimer's disease treatment. J. Neurosci. 2012, 32, 5144-5150.
9. Ho, L., Ferruzzi, M. G., Janle, E. M., Wang, J. et al., Identification of brain-targeted bioactive dietary quercetin-3-O-glucuronide as a novel intervention for Alzheimer's disease. FASEB J.2013, 27, 769-781.
10. Drouin, A., Bolduc, V., Thorin-Trescases, N., Bélanger, E. et al., Catechin treatment improves cerebrovascular flow-mediated dilation and learning abilities in atherosclerotic mice. Am. J. Physiol. Heart Circ. Physiol. 2011, 300, H1032-H1043.
11. Hollecker, L., Pinna, M., Filippino, G., Scrugli, S. et al., Simultaneous determination of polyphenolic compounds in red and white grapes grown in Sardinia by high performance liquid chromatography-electron spray ionisation-mass spectrometry. J. Chromatog. A. 2009, 1216, 3402-3408.
12. Lee, K. W., Kim, Y. J., Kim, D. O., Lee, H. J. et al., Major phenolics in apple and their contribution to the total antioxidant capacity. J. Agric. Food Chem. 2003, 51, 6516-6520.
13. Latti, A. K., Riihinen, K. R., Jaakola, L., Phenolic compounds in berries and flowers of a natural hybrid between bilberry and lingonberry (Vaccinium x intermedium Ruthe). Phytochemistry 2011, 72, 810-815.
14. Liang, Z., Yang, Y. Cheng, L., Zhong, G. Y., Characterization of polyphenolic metabolites in the seeds of Vitis germplasm. J. Agric. Food Chem 2012, 60, 1291-1299.
15. Scalbert, A., Williamson, G., Dietary intake and bioavailability of polyphenols. J. Nutr. 2000, 130 (8S Suppl), 2073S-2085S.
16. Manach, C., Williamson, G., Morand, C., Scalbert, A. et al., Bioavailability and bioefficacy of polyphenols in humans. I. Review of 97 bioavailability studies. Am. J. Clin. Nutr. 2005, 81 (1 Suppl), 230S-242S.
17. Nakagawa, K., Miyazawa, T., Absorption and distribution of tea catechin, (-)-epigallocatechin-3-gallate, in the rat. J. Nutr. Sci. Vitaminol. (Tokyo) 1997, 43, 679-684.
18. Abd El Mohsen, M. M., Kuhnle, G., Rechner, A. R., Schroeter, H. et al., Uptake and metabolism of epicatechin and its access to the brain after oral ingestion. Free Radic. Biol. Med. 2002, 33, 1693-1702.
19. Ferruzzi, M. G., Lobo, J. K., Janle, E. M., Cooper, B. et al., Bioavailability of gallic acid and catechins from grape seed polyphenol extract is improved by repeated dosing in rats: implications for treatment in Alzheimer's disease. J. Alzheimers Dis. 2009, 18, 113-124.
20. Prasain, J. K., Peng, N., Dai, Y., Moore, R. et al., Liquid chromatography tandem mass spectrometry identification of proanthocyanidins in rat plasma after oral administration of grape seed extract. Phytomedicine 2009, 16, 233-243.
21. Serra, A., Macia, A., Rubió, L., Anglès, N. et al., Distribution of procyanidins and their metabolites in rat plasma and tissues in relation to ingestion of procyanidin-enriched or procyanidin-rich cocoa creams. Eur. J. Nutr. 2012, 52, 1029-1038.
22. de Boer, V. C., Dihal, A. A., van der Woude, H., Arts, I. C. et al., Tissue distribution of quercetin in rats and pigs. J. Nutr. 2005, 135, 1718-1725.
23. Percival, S. S., Commentary on: tissue distribution of quercetin in rats and pigs. J. Nutr. 2005, 135, 1617-1618.
24. Bieger, J., Cermak, R., Blank R., de Boer, V. C. et al., Tissue distribution of quercetin in pigs after long-term dietary supplementation. J. Nutr. 2008, 138, 1417-1420.
25. Conrad, M. S., Dilger, R. N., Johnson, R. W., Brain growth of the domestic pig (Sus scrofa) from 2 to 24 weeks of age: a longitudinal MRI study. Dev Neurosci. 2012, 34, 291-298.
26. Conrad, M. S., Dilger, R. N., Nickolls, A., Johnson, R. W., Magnetic resonance imaging of the neonatal piglet brain. Pediatr. Res. 2012, 71, 179-184.
27. Patterson, J. K., Lei, X. G., Miller, D. D., The pig as an experimental model for elucidating the mechanisms governing dietary influence on mineral absorption. Exp. Biol. Med. (Maywood) 2008, 233, 651-664.
28. Song, B. J., Jouni, Z. E., Ferruzzi, M. G., Assessment of phytochemical content in human milk during different stages of lactation. Nutrition 2013, 29, 195-202.
29. Song, B. J., Sapper, T. N., Burtch, C. E., Brimmer, K. et al., Photo- and thermodegradation of anthocyanins from grape and purple sweet potato in model beverage systems. J. Agric. Food Chem. 2013, 61, 1364-1372.
30. Waterhouse, A. L., Determination of Total Phenolics, in Current Protocols in Food Analytical Chemistry, I1.1.1-I1.1.8, Wrolstad, R.E., Wiley, 2001.
31. U.S. Department of Health and Human Services, Food and Drug Administration Center for Drug Evaluation and Research (CDER), Estimating the Maximum Safe Starting Dose in Initial Clinical Trials for Therapeutics in Adult Healthy Volunteers. (2005).
32. Marchant-Forde, J. N, Matthews, D. L., Poletto R., McCain R. R. et al., Plasma cortisol and noradrenalin concentrations in pigs: automated sampling of freely moving pigs housed in the PigTurn® versus manually sampled and restrained pigs. Animal Welfare 2012, 21, 197-205.
33. Blount, J. W., Redan, B. W., Ferruzzi, M. G., Reuhs, B. L. et al., Synthesis and quantitative analysis of plasma-targeted metabolites of catechin and epicatechin. J. Agric. Food Chem. 2015, 63, 2233-2240.
34. Može, S., Polak, T., Gašperlin, L., Koron, D. et al., Phenolics in Slovenian bilberries (Vaccinium myrtillus L.) and blueberries (Vaccinium corymbosum L.). J. Agric. Food Chem. 2011, 59, 6998-7004.
35. Wang, J., Tang, C., Ferruzzi, M. G., Gong, B. et al., Role of Standardized Grape Polyphenol Preparation as a novel treatment to improve synaptic plasticity through attenuation of features of metabolic syndrome. Mol. Nutr. Food Res. 2013, 57, 2091-2102.
36. Zhang, Z., Kou, X., McLaughlin J., Comparison of HPLC methods for determination of anthocyanins and anthocyanidins in bilberry extracts. J. Agric. Food Chem. 2004, 52, 688-691.
37. Wu, X., Prior, R. L., Identification and characterization of anthocyanins by high-performance liquid chromatography-electrospray ionization-tandem mass spectrometry in common foods in the United States: vegetables, nuts, and grains. J. Agric. Food Chem. 2005, 53, 3101-3113.
38. Lee, J. H., Kang, N. S., Shin S-O., Shin, S-H. et al., Characterisation of anthocyanins in the black soybean (Glycine max L.) by HPLC-DAD-ESI/MS analysis. Food Chem. 2009, 112, 226-231.
39. Ha, T. J., Lee, M. H., Park, C. H., Pae, S. B. et al., Identification and characterization of anthocyanins in yard-long beans (Vigna unguiculata ssp. sesquipedalis L.) by High-performance liquid chromatography with diode array detection and electrospray ionization/mass spectrometry (HPLC-DAD-ESI/MS) analysis. J. Agric. Food Chem. 2010, 58, 2571-2576.
40. Silberberg, M., Morand, C., Manach, C., Scalbert, A. et al., Co-administration of quercetin and catechin in rats alters their absorption but not their metabolism. Life Sci. 2005, 77, 3156-3167.
41. Pérez-Jiménez, J., Hubert, J., Hooper, L., Cassidy, A., Urinary metabolites as biomarkers of polyphenol intake in humans: a systematic review. Am. J. Clin. Nutr. 2010, 92, 801-809.
42. Serra, A., Macià, A., Rubió, L., Anglès, N. et al., Distribution of procyanidins and their metabolites in rat plasma and tissues in relation to ingestion of procyanidin-enriched or procyanidin-rich cocoa creams. Eur. J. Nutr. 2013, 52, 1029-1038.
43. de Boer, V. C., Dihal, A. A., van der Woude, H., Arts, I. C. et al., Tissue distribution of quercetin in rats and pigs. J. Nutr. 2005, 135, 1718-1725.
44. Gee, J. M., DuPont, M. S., Day, A. J., Plumb, G. W. et al., Intestinal transport of quercetin glycosides in rats involves both deglycosylation and interaction with the hexose transport pathway." J. Nutr. 2000, 130, 2765-2771.
45. Moon, J. H., Tsushida, T., Nakahara, K., Terao, J., Identification of quercetin 3-O-beta-D-glucuronide as an antioxidative metabolite in rat plasma after oral administration of quercetin. Free Radic. Biol. Med. 2001, 30, 1274-1285.
46. Day, A. J., Williamson G., Biomarkers for exposure to dietary flavonoids: a review of the current evidence for identification of quercetin glycosides in plasma. Br. J. Nutr. 2001, 1 (86 Suppl.), S105-S110.
47. Janisch, K. M., Williamson, G., Needs, P., Plumb, G. W., Properties of quercetin conjugates: modulation of LDL oxidation and binding to human serum albumin. Free Radic. Res. 2004, 38, 877-884.
48. Ader, P., Wessmann, A., Wolffram, S., Bioavailability and metabolism of the flavonol quercetin in the pig. Free Radic. Biol. Med. 2000, 28, 1056-1067.
49. Lesser, S., Cermak, R., Wolffram, S., Bioavailability of quercetin in pigs is influenced by the dietary fat content. J. Nutr. 2004, 134, 1508-1511.
50. 13C-tracer study. Am. J. Clin. Nutr. 2013, 97, 995-1003.
51. González-Barrio, R., Borges, G., Mullen, W., Crozier, A., Bioavailability of anthocyanins and ellagitannins following consumption of raspberries by healthy humans and subjects with an ileostomy. J. Agric. Food Chem. 2010, 58, 3933-3939.
52. Felgines, C., Texier, O., Garcin, P., Besson, C., Tissue distribution of anthocyanins in rats fed a blackberry anthocyanin-enriched diet. Mol. Nutr. Food Res. 2009, 53, 1098-1103.
53. Passamonti, S., Vrhovsek, U., Vanzo, A., Mattivi, F., The stomach as a site for anthocyanins absorption from food. FEBS Lett. 2003, 544, 210-213.
54. Talavera, S., Felgines, C. Texier, O., Besson, C. et al., Anthocyanins are efficiently absorbed from the stomach in anesthetized rats. J. Nutr 2003, 133, 4178-4182.
55. de Ferrars, R. M., Czank, C., Zhang, Q., Botting, N. P., The pharmacokinetics of anthocyanins and their metabolites in humans. Br. J. Pharmacol. 2014, 171, 3268-3282.
56. Del Bo, C., Ciappellano, S., Klimis-Zacas, D., Martini, D. et al., Anthocyanin absorption, metabolism, and distribution from a wild blueberry-enriched diet (Vaccinium angustifolium) is affected by diet duration in the Sprague-Dawley rat. J Agric. Food Chem. 2010, 58, 2491-2497.
57. Juan, M. E., Maijo, M., Planas, J. M., Quantification of trans-resveratrol and its metabolites in rat plasma and tissues by HPLC. J. Pharm. Biomed. Anal. 2010, 51, 391-398.
58. Ishisaka, A., Ichikawa, S., Sakakibara, H., Piskula, M. K. et al., Accumulation of orally administered quercetin in brain tissue and its antioxidative effects in rats. Free Radic. Biol. Med. 2011, 51, 1329-1336.
59. Andres-Lacueva, C., Shukitt-Hale, B., Galli, R. L., Jauregui, O. et al., Anthocyanins in aged blueberry-fed rats are found centrally and may enhance memory." Nutr. Neurosci. 2005, 8, 111-120.
60. Milbury, P. E., Kalt, W., Xenobiotic metabolism and berry flavonoid transport across the blood-brain barrier. J. Agric. Food Chem. 2010, 58, 3950-3956.
61. Kalt, W., Blumberg, J. B., McDonald, J. E., Vinqvist-Tymchuk, M. R. et al., "Identification of anthocyanins in the liver, eye, and brain of blueberry-fed pigs." J. Agric. Food Chem. 2008, 56, 705-712.
62. Friden, M., Ljungqvist, H., Middleton, B., Bredberg, U. et al., Improved measurement of drug exposure in the brain using drug-specific correction for residual blood. J. Cereb. Blood Flow Metab. 2010, 30, 150-161.
63. Kirakosyan, A., Seymour, E. M., Wolforth, J., McNish, R. et al., Tissue bioavailability of anthocyanins from whole tart cherry in healthy rats. Food Chem. 2015, 171, 26-31.