Bioavailability of resveratrol: Possibilities for enhancement

Journal of Herbal Medicine

Volumn 11, Issue , 2018, Pages 71-77

  de Vries, Konrad ^a   Strydom, Morné ^b   Steenkamp, Vanessa ^a  

^a UNIVERSITY OF PRETORIA   (South Africa)

^b Synexus Clinical Research South Africa/Rota Consortium   (South Africa)

Author keywords

Bioavailability; Clinical trials; Efficacy; Resveratrol

Indexed keywords

DRUG METABOLITE; PHYTOCHEMICAL; PRODRUG; RESVERATROL;

DRUG BIOAVAILABILITY; DRUG FORMULATION; DRUG POTENTIATION; HUMAN; NANOTECHNOLOGY; NONHUMAN; PRIORITY JOURNAL; REVIEW; SYSTEMATIC REVIEW;

EID: 85030783756     PISSN: 22108033     EISSN: 22108041     Source Type: Journal    
DOI: 10.1016/j.hermed.2017.09.002     Document Type: Review

References (75)

1. Almeida, L., Vaz-da-Silva, M., Falcão, A., Soares, E., Costa, R., Loureiro, A.I., Fernandes-Lopes, C., Rocha, J.F., Nunes, T., Wright, L., Pharmacokinetic and safety profile of trans-resveratrol in a rising multiple-dose study in healthy volunteers. Mol. Nutr. Food Res. 53 (2009), S7–S15.
2. Amiot, M., Riva, C., Vinet, A., Effects of dietary polyphenols on metabolic syndrome features in humans: a systematic review. Obes. Rev. 17 (2016), 573–586.
3. Ansari, K.A., Vavia, P.R., Trotta, F., Cavalli, R., Cyclodextrin-based nanosponges for delivery of resveratrol: in vitro characterisation, stability, cytotoxicity and permeation study. AAPS PharmSciTech. 12 (2011), 279–286.
4. Artero, A., Artero, A., Tarín, J.J., Cano, A., The impact of moderate wine consumption on health. Maturitas 80 (2015), 3–13.
5. Azachi, M., Yatuv, R., Katz, A., Hagay, Y., Danon, A., A novel red grape cells complex: health effects and bioavailability of natural resveratrol. Int. J. Food Sci. Nutr. 65 (2014), 848–855.
6. Banu, S.K., Stanley, J.A., Sivakumar, K.K., Arosh, J.A., Burghardt, R.C., Resveratrol protects the ovary against chromium-toxicity by enhancing endogenous antioxidant enzymes and inhibiting metabolic clearance of estradiol. Toxicol. Appl. Pharmacol. 303 (2016), 65–78.
7. Barnes, P.J., New anti-inflammatory targets for chronic obstructive pulmonary disease. Nat. Rev. Drug Discov. 12 (2013), 543–559.
8. Bashmakov, Y.K., Assaad-Khalil, S.H., Abou Seif, M., Udumyan, R., Megallaa, M., Rohoma, K.H., Zeitounet, M., Petyaev, I.M., Resveratrol promotes foot ulcer size reduction in type 2 diabetes patients. ISRN Endocrinol., 2014.
9. Bastianetto, S., Ménard, C., Quirion, R., Neuroprotective action of resveratrol. Biochim. Biophys. Acta 1852 (2015), 1195–1201.
10. Bhullar, K.S., Udenigwe, C.C., Clinical evidence of resveratrol bioactivity in cardiovascular disease. Current Opin. Food Sci. 8 (2016), 68–73.
11. Blanchard, O.L., Friesenhahn, G., Javors, M.A., Smoliga, J.M., Development of a lozenge for oral transmucosal delivery of trans-resveratrol in humans: proof of concept. PLoS One, 9, 2014, e90131.
12. Calabrese, E.J., Mattson, M.P., Calabrese, V., Resveratrol commonly displays hormesis: occurrence and biomedical significance. Hum. Exp. Toxicol. 29 (2010), 980–1015.
13. Calabrese, E.J., Resveratrol: an assessment of its dose response an introduction. Hum. Exp. Toxicol., 29, 2010, 977.
14. Chachay, V.S., Macdonald, G.A., Martin, J.H., Whitehead, J.P., O'Moore–Sullivan, T.M., Lee, P., Franklin, M., Klein, K., Taylor, P.J., Ferquson, M., Coombes, J.S., Thomas, G.P., Cowin, G.J., Kirkpatrick, C.M., Prins, J.B., Hickman, I.J., Resveratrol does not benefit patients with nonalcoholic fatty liver disease. Clin. Gastroenterol. 12:2092–2103 (2014), e1–e6.
15. Chen, C.-J., Yu, W., Fu, Y.-C., Wang, X., Li, J.-L., Wang, W., Resveratrol protects cardiomyocytes from hypoxia-induced apoptosis through the SIRT1–FoxO1 pathway. Biochem. Biophys. Res. Commun. 378 (2009), 389–393.
16. Chen, W., Yeo, S.C.M., Elhennawy, M.G.A.A., Xiang, X., Lin, H.-S., Determination of naturally occurring resveratrol analog trans-4, 4′-dihydroxystilbene in rat plasma by liquid chromatography-tandem mass spectrometry: application to a pharmacokinetic study. Anal. Bioanal. Chem. 407 (2015), 5793–5801.
17. Chen, W., Yeo, S.C.M., Elhennawy, M.G.A.A., Lin, H.-S., Oxyresveratrol: a bioavailable dietary polyphenol. J. Funct. Foods. 22 (2016), 122–131.
18. Choo, Q.-Y., Yeo, S.C.M., Ho, P.C., Tanaka, Y., Lin, H.-S., Pterostilbene surpassed resveratrol for anti-inflammatory application: potency consideration and pharmacokinetics perspective. J. Funct. Foods 11 (2014), 352–362.
19. Crescente, M., Jessen, G., Momi, S., Höltje, H.-D., Gresele, P., Cerletti, C., de Gaetano, G., Interactions of gallic acid, resveratrol, quercetin and aspirin at the platelet cyclooxygenase-1 level. Thromb. Haemost. 102 (2009), 336–346.
20. Das, S., Lin, H.-S., Ho, P.C., Ng, K.-Y., The impact of aqueous solubility and dose on the pharmacokinetic profiles of resveratrol. Pharm. Res. 25 (2008), 2593–2600.
21. De Amicis, F., Giordano, F., Vivacqua, A., Pellegrino, M., Panno, M.L., Tramontano, D., Fuqua, S.A.W., Andò, S., Resveratrol, through NF-Y/p53/Sin3/HDAC1 complex phosphorylation, inhibits estrogen receptor α gene expression via p38 MAPK/CK2 signaling in human breast cancer cells. FASEB J. 25 (2011), 3695–3707.
22. De Leo, A., Arena, G., Stecca, C., Raciti, M., Mattia, E., Resveratrol inhibits proliferation and survival of Epstein Barr virus-infected Burkitt's lymphoma cells depending on viral latency program. Mol. Cancer Res. 9 (2011), 1346–1355.
23. Faghihzadeh, F., Adibi, P., Hekmatdoost, A., The effects of resveratrol supplementation on cardiovascular risk factors in patients with non-alcoholic fatty liver disease: a randomised, double-blind, placebo-controlled study. Br. J. Nutr. 114 (2015), 796–803.
24. Feng, M., Zhong, L.-X., Zhan, Z.-Y., Huang, Z.-H., Xiong, J.-P., Resveratrol treatment inhibits proliferation of and induces apoptosis in human colon cancer cells. Med. Sci. Monit., 22, 2016, 1101.
25. Fernández, A.F., Fraga, M.F., The effects of the dietary polyphenol resveratrol on human healthy aging and lifespan. Epigenetics 6 (2011), 870–874.
26. Giacosa, A., Barale, R., Bavaresco, L., Faliva, M.A., Gerbi, V., La Vecchia, C., Negri, E., Opizzi, A., Perna, S., Pezzotti, M., Mediterranean way of drinking and longevity. Crit. Rev. Food Sci. Nutr. 56 (2016), 635–640.
27. Heebøll, S., Kreuzfeldt, M., Hamilton-Dutoit, S., Kjær Poulsen, M., Stødkilde-Jørgensen, H., Møller, H.J., Jessen, N., Thorsen, K., Kristina Hellberg, Y., Bønløkke Pedersen, S., Placebo-controlled, randomised clinical trial: high-dose resveratrol treatment for non-alcoholic fatty liver disease. Scand. J. Gastroenterol. 51 (2016), 456–464.
28. Jin, F., Wu, Q., Lu, Y.-F., Gong, Q.-H., Shi, J.-S., Neuroprotective effect of resveratrol on 6-OHDA-induced Parkinson's disease in rats. Eur. J. Pharmacol. 600 (2008), 78–82.
29. Johnson, J.J., Nihal, M., Siddiqui, I.A., Scarlett, C.O., Bailey, H.H., Mukhtar, H., Ahmad, N., Enhancing the bioavailability of resveratrol by combining it with piperine. Mol. Nutr. Food Res. 55 (2011), 1169–1176.
30. Kang, L., Heng, W., Yuan, A., Baolin, L., Fang, H., Resveratrol modulates adipokine expression and improves insulin sensitivity in adipocytes: relative to inhibition of inflammatory responses. Biochimie 92 (2010), 789–796.
31. Kjær, T.N., Ornstrup, M.J., Poulsen, M.M., Jørgensen, J.O., Hougaard, D.M., Cohen, A.S., Neqhabat, S., Richelsen, B., Pedersen, S.B., Resveratrol reduces the levels of circulating androgen precursors but has no effect on, testosterone, dihydrotestosterone, PSA levels or prostate volume. A 4-month randomised trial in middle-aged men. Prostate 75 (2015), 1255–1263.
32. Koide, K., Osman, S., Garner, A.L., Song, F., Dixon, T., Greenberger, J.S., Epperly, M.W., The use of 3, 5, 4′-Tri-O-acetylresveratrol as a potential prodrug for Resveratrol protects mice from γ-irradiation-induced death. ACS Med. Chem. Lett. 2 (2011), 270–274.
33. Liang, L., Liu, X., Wang, Q., Cheng, S., Zhang, S., Zhang, M., Pharmacokinetics, tissue distribution and excretion study of resveratrol and its prodrug 3, 5, 4′-tri-O-acetylresveratrol in rats. Phytomedicine 20 (2013), 558–563.
34. Lin, H.S., Ho, P.C., Preclinical pharmacokinetic evaluation of resveratrol trimethyl ether in Sprague-Dawley rats: the impacts of aqueous solubility, dose escalation, food and repeated dosing on oral bioavailability. J. Pharm. Sci. 100 (2011), 4491–4500.
35. Lin, C.-T., Sun, X.-Y., Lin, A.-X., Supplementation with high-dose trans-resveratrol improves ultrafiltration in peritoneal dialysis patients: a prospective, randomized, double-blind study. Ren. Fail. 38 (2016), 214–221.
36. Ma, C., Wang, Y., Dong, L., Li, M., Cai, W., Anti-inflammatory effect of resveratrol through the suppression of NF-κB and JAK/STAT signaling pathways. Acta Biochem. Biophys. Sin. 47 (2015), 207–213.
37. Mukherjee, S., Dudley, J.I., Das, D.K., Dose-dependency of resveratrol in providing health benefits. Dose Response 8 (2010), 478–500.
38. Mulero, J., Abellán, J., Zafrilla, P., Amores, D., Hernández Sánchez, P., Bioactive substances with preventive effect in cardiovascular diseases. Nutr. Hosp. 32 (2015), 1462–1467.
39. Neves, A.R., Lúcio, M., Martins, S., Lima, J., Reis, S., Novel resveratrol nanodelivery systems based on lipid nanoparticles to enhance its oral bioavailability. Int. J. Nanomed. 8 (2013), 177–187.
40. Ornstrup, M.J., Harsløf, T., Kjær, T.N., Langdahl, B.L., Pedersen, S.B., Resveratrol increases bone mineral density and bone alkaline phosphatase in obese men: a randomized placebo-controlled trial. J. Clin. Endocrinol. Metab. 99 (2014), 4720–4729.
41. Osmond, G.W., Augustine, C.K., Zipfel, P.A., Padussis, J., Tyler, D.S., Enhancing melanoma treatment with resveratrol. J. Surg. Res. 172 (2012), 109–115.
42. Palsamy, P., Subramanian, S., Ameliorative potential of resveratrol on proinflammatory cytokines, hyperglycemia mediated oxidative stress, and pancreatic β-cell dysfunction in streptozotocin-nicotinamide-induced diabetic rats. J. Cell. Physiol. 224 (2010), 423–432.
43. Park, S.-J., Ahmad, F., Philp, A., Baar, K., Williams, T., Luo, H., Ke, H., Rehmann, H., Taussig, R., Brown, A.L., Resveratrol ameliorates aging-related metabolic phenotypes by inhibiting cAMP phosphodiesterases. Cell 148 (2012), 421–433.
44. Park, S.Y., Chae, S.Y., Park, J.O., Lee, K.J., Park, G., Gold-conjugated resveratrol nanoparticles attenuate the invasion and MMP-9 and COX-2 expression in breast cancer cells. Oncol. Rep. 35 (2016), 3248–3256.
45. Patel, K.R., Brown, V.A., Jones, D.J., Britton, R.G., Hemingway, D., Miller, A.S., West, K.P., Booth, T.D., Perloff, M., Crowell, J.A., Clinical pharmacology of resveratrol and its metabolites in colorectal cancer patients. Cancer Res. 70 (2010), 7392–7399.
46. Patel, K.R., Andreadi, C., Britton, R.G., Horner-Glister, E., Karmokar, A., Sale, S., Brown, V.A., Brenner, D.E., Singh, R., Steward, W.P., Sulfate metabolites provide an intracellular pool for resveratrol generation and induce autophagy with senescence. Sci. Trans. Med., 5, 2013, 205ra133.
47. Riccioni, G., Gammone, M.A., Tettamanti, G., Bergante, S., Pluchinotta, F.R., D'Orazio, N., Resveratrol and anti-atherogenic effects. Int. J. Food Sci. Nutr. 66 (2015), 603–610.
48. Sahebkar, A., Serban, C., Ursoniu, S., Wong, N.D., Muntner, P., Graham, I.M., Mikhailidis, D.P., Rizzo, M., Rysz, J., Sperling, L.S., Lack of efficacy of resveratrol on C-reactive protein and selected cardiovascular risk factors–Results from a systematic review and meta-analysis of randomized controlled trials. Int. J. Cardiol. 189 (2015), 47–55.
49. Samsami-kor, M., Daryani, N.E., Asl, P.R., Hekmatdoost, A., Anti-inflammatory effects of resveratrol in patients with ulcerative colitis: a randomized, double-blind, placebo-controlled pilot study. Arch. Med. Res. 46 (2015), 280–285.
50. Sanna, V., Roggio, A.M., Siliani, S., Piccinini, M., Marceddu, S., Mariani, A., Sechi, M., Development of novel cationic chitosan-and anionic alginate-coated poly (D, L-lactide-co-glycolide) nanoparticles for controlled release and light protection of resveratrol. Int. J. Nanomed. 7 (2012), 5501–5516.
51. Sanna, V., Pala, N., Dessì, G., Manconi, P., Mariani, A., Dedola, S., Rassu, M., Crosio, C., Iaccarino, C., Sechi, M., Single-step green synthesis and characterization of gold-conjugated polyphenol nanoparticles with antioxidant and biological activities. Int. J. Nanomed., 9, 2014, 4935.
52. Siddiqui, I.A., Sanna, V., Impact of nanotechnology on the delivery of natural products for cancer prevention and therapy. Mol. Nutr. Food Res. 60 (2016), 1330–1341.
53. Smoliga, J.M., Blanchard, O., Enhancing the delivery of resveratrol in humans: if low bioavailability is the problem, what is the solution?. Molecules 19 (2014), 17154–17172.
54. Smoliga, J.M., Baur, J.A., Hausenblas, H.A., Resveratrol and health?a comprehensive review of human clinical trials. Mol. Nutr. Food Res. 55 (2011), 1129–1141.
55. Teskač, K., Kristl, J., The evidence for solid lipid nanoparticles mediated cell uptake of resveratrol. Int. J. Pharm. 390 (2010), 61–69.
56. Thazhath, S.S., Wu, T., Bound, M.J., Checklin, H.L., Standfield, S., Jones, K.L., Horowitz, M., Rayner, C.K., Administration of resveratrol for 5 wk has no effect on glucagon-like peptide 1 secretion, gastric emptying, or glycemic control in type 2 diabetes: a randomized controlled trial. Am. J. Clin. Nutr. 103 (2016), 66–70.
57. Tomayko, E.J., Cachia, A.J., Chung, H.R., Wilund, K.R., Resveratrol supplementation reduces aortic atherosclerosis and calcification and attenuates loss of aerobic capacity in a mouse model of uremia. J. Med. Food 17 (2014), 278–283.
58. Trotta, V., Lee, W.-H., Loo, C.-Y., Haghi, M., Young, P.M., Scalia, S., Traini, D., In vitro biological activity of resveratrol using a novel inhalable resveratrol spray-dried formulation. Int. J. Pharm. 491 (2015), 190–197.
59. Trotta, V., Lee, W.-H., Loo, C.-Y., Young, P.M., Traini, D., Scalia, S., Co-spray dried resveratrol and budesonide inhalation formulation for reducing inflammation and oxidative stress in rat alveolar macrophages. Eur. J. Pharm. Sci. 86 (2016), 20–28.
60. Turner, R.S., Thomas, R.G., Craft, S., Van Dyck, C.H., Mintzer, J., Reynolds, B.A., Brewer, J.B., Rissman, R.A., Raman, R., Aisen, P.S., A randomized, double-blind, placebo-controlled trial of resveratrol for Alzheimer disease. Neurology 85 (2015), 1383–1391.
61. Vislocky, L.M., Fernandez, M.L., Biomedical effects of grape products. Nutr. Rev. 68 (2010), 656–670.
62. Walle, T., Hsieh, F., DeLegge, M.H., Oatis, J.E., Walle, U.K., High absorption but very low bioavailability of oral resveratrol in humans. Drug Metab. Dispos. 32 (2004), 1377–1382.
63. Watkins, R., Wu, L., Zhang, C., Davis, R.M., Xu, B., Natural product-based nanomedicine: recent advances and issues. Int. J. Nanomed., 10, 2015, 6055.
64. Wightman, E.L., Reay, J.L., Haskell, C.F., Williamson, G., Dew, T.P., Kennedy, D.O., Effects of resveratrol alone or in combination with piperine on cerebral blood flow parameters and cognitive performance in human subjects: a randomised double-blind, placebo-controlled, cross-over investigation. Br. J. Nutr. 112 (2014), 203–213.
65. Wightman, E.L., Haskell-Ramsay, C.F., Reay, J.L., Williamson, G., Dew, T., Zhang, W., Kennedy, D.O., The effects of chronic trans-resveratrol supplementation on aspects of cognitive function, mood, sleep, health and cerebral blood flow in healthy young humans. Br. J. Nutr. 114 (2015), 1427–1437.
66. Witte, A.V., Kerti, L., Margulies, D.S., Flöel, A., Effects of resveratrol on memory performance, hippocampal functional connectivity, and glucose metabolism in healthy older adults. J. Neurosci. 34 (2014), 7862–7870.
67. Wong, R.H., Berry, N.M., Coates, A.M., Buckley, J.D., Bryan, J., Kunz, I., Howe, P.R., Chronic resveratrol consumption improves brachial flow-mediated dilatation in healthy obese adults. J. Hypertens. 31 (2013), 1819–1827.
68. Wong, R., Nealon, R., Scholey, A., Howe, P., Low dose resveratrol improves cerebrovascular function in type 2 diabetes mellitus. Nutr. Metab. Cardiovasc. Dis. 26 (2016), 393–399.
69. Yeo, S.C.M., Ho, P.C., Lin, H.S., Pharmacokinetics of pterostilbene in Sprague-Dawley rats: the impacts of aqueous solubility, fasting, dose escalation, and dosing route on bioavailability. Mol. Nutr. Food Res. 57 (2013), 1015–1025.
70. Yeo, S.C.M., Fenwick, P.S., Barnes, P.J., Lin, H.S., Donnelly, L.E., Isorhapontigenin, a bioavailable dietary polyphenol, suppresses airway epithelial cell inflammation through a corticosteroid-independent mechanism. Br. J. Pharmacol. 174 (2017), 2043–2059.
71. Yiu, E.M., Tai, G., Peverill, R.E., Lee, K.J., Croft, K.D., Mori, T.A., Scheiber-Mojdehkar, B., Sturm, B., Praschberger, M., Vogel, A.P., An open-label trial in Friedreich ataxia suggests clinical benefit with high-dose resveratrol, without effect on frataxin levels. J. Neurol. 262 (2015), 1344–1353.
72. Zhang, F., Wang, H., Wu, Q., Lu, Y., Nie, J., Xie, X., Shi, J., Resveratrol protects cortical neurons against microglia-mediated neuroinflammation. Phytother. Res. 27 (2013), 344–349.
73. Zhu, W., Qin, W., Zhang, K., Rottinghaus, G.E., Chen, Y.-C., Kliethermes, B., Sauter, E.R., Trans-resveratrol alters mammary promoter hypermethylation in women at increased risk for breast cancer. Nutr. Cancer 64 (2012), 393–400.
74. Zortea, K., Franco, V.C., Francesconi, L.P., Cereser, K.M., Lobato, M.I.R., Belmonte-de-Abreu, P.S., Resveratrol supplementation in schizophrenia patients: a randomized clinical trial evaluating serum glucose and cardiovascular risk factors. Nutrients, 8, 2016, 73.
75. van der Made, S.M., Plat, J., Mensink, R.P., Resveratrol does not influence metabolic risk markers related to cardiovascular health in overweight and slightly obese subjects: a randomized, placebo-controlled crossover trial. PLoS One, 10, 2015, e0118393.