Multiple effects of grape seed polyphenolics to prevent metabolic diseases

Abstract

Obesity is increasing in developing countries. Population studies show a relationship between affluence and obesity. Changing food intake patterns with affluence such as preference for foods with less astringent polyphenolic compounds and dietary fibers may increase risk of metabolic dysfunctions due to caloric imbalance. Animal models of obesity consistently show that grape seed procyanidins prevent increases in body and abdo- minal adipose weight gain, plasma cholesterol, liver weight gain and inflammation in animals on high fat diets. The mechanisms are not clear because the oral intake of procyanidins results in pleiotropic interactions with proteins in the mouth, stomach, small intestine, cecum and colon that affect the rate of digestion of bioavailability of macronutrients, sterols, and dietary fiber. Procyanidins also bind bile acids and reduce intestinal permeability to inflammatory bacterial cell wall fragment. Procyanidins are not degraded or metabolized until reaching the lower gut where they can be metabolized into phenolic acids by gut bacteria. While they are metabolized by gut bacteria, they also alter total numbers and distribution of phyla and species of gut bacteria. Gut bacteria are recognized as significant contributors to obesity and obesity related metabolic diseases. The review examines the different pleiotropic effects of grape seed procyanidins that have a significant effect on metabolic disease in animal models of obesity.

Keywords

grape seed / obesity / procyanidins / high fat / microbiota / animal models

References

[1] Caputo T, Gilardi F, Desvergne B. From chronic overnutrition to metaflammation and insulin resistance: adipose tissue and liver contributions. FEBS Letters, 2017, 591(19): 3061–3088

[2] Mancuso P. The role of adipokines in chronic inflammation. Immuno Targets and Therapy, 2016, 5: 47–56

[3] Hamilton M K, Raybould H E. Bugs, guts and brains, and the regulation of food intake and body weight. International Journal of Molecular Sciences 2016, 6 (S1): 8–14

[4] Kumari M, Kozyrskyj A L. Gut microbial metabolism defines host metabolism: an emerging perspective in obesity and allergic inflammation. Obesity Reviews: an Official Journal of the International Association for the Study of Obesity, 2017, 18(1): 18–31

[5] Wen L, Duffy A. Factors influencing the gut microbiota, inflammation, and type 2 diabetes. Journal of Nutritional Biochemistry, 2017, 147(7): 1468S–1475S

[6] Hruby A, Hu F B. The epidemiology of obesity: a big picture. PharmacoEconomics, 2015, 33(7): 673–689

[7] Peng W, Berry E M. Global nutrition 1990–2015: a shrinking hungry, and expanding fat world. PLoS One, 2018, 13(3): e0194821

[8] Araújo J R, Tomas J, Brenner C, Sansonetti P J. Impact of high-fat diet on the intestinal microbiota and small intestinal physiology before and after the onset of obesity. Biochimie, 2017, 141: 97–106

[9] King H, Aubert R E, Herman W H. Global burden of diabetes, 1995–2025: prevalence, numerical estimates, and projections. Diabetes Care, 1998, 21(9): 1414–1431

[10] NCD Risk Factor Collaboration (NCD-RisC). Trends in adult body-mass index in 200 countries from 1975 to 2014: a pooled analysis of 1698 population-based measurement studies with 19.2 million participants. Lancet, 2016, 387(10026): 1377–1396

[11] Wang H J, Zhang B, Du W W, Liu A D, Zhang J G, Wang Z H, Su C, Ma Y X, Zhai F Y. Trends of the dietary fiber intake among Chinese aged 18–45 in nine provinces (autonomous region) from 1989 to 2006. Chinese Journal of Preventive Medicine, 2011, 45(4): 318–322

[12] Xiao Y, Su C, Ouyang Y, Zhang B. Trends of vegetables and fruits consumption among Chinese adults aged 18 to 44 years old from 1991 to 2011. Chinese Journal of Epidemiology, 2015, 36(3): 232–236

[13] Ngamukote S, Mäkynen K, Thilawech T, Adisakwattana S. Cholesterol-lowering activity of the major polyphenols in grape seed. Molecules, 2011, 16(6): 5054–5061

[14] Prior R L, Gu L. Occurrence and biological significance of proanthocyanidins in the American diet. Phytochemistry, 2005, 66(18): 2264–2280

[15] Fuleki T, Ricardo-da-Silva J M. Catechin and procyanidin composition of seeds from grape cultivars grown in Ontario. Journal of Agricultural and Food Chemistry, 1997, 45(4): 1156–1160

[16] Arranz S, Saura-Calixto F, Shaha S, Kroon P A. High contents of nonextractable polyphenols in fruits suggest that polyphenol contents of plant foods have been underestimated. Journal of Agricultural and Food Chemistry, 2009, 57(16): 7298–7303

[17] Perez-Jimenez J, Arranz S, Saura-Calixto F. Proanthocyanidin content in foods is largely underestimated in the literature data: an approach to quantification of the missing proanthocyanidins. Food Research International, 2009, 42(10): 1381–1388

[18] Weber H A, Hodges A E, Guthrie J R, O’Brien B M, Robaugh D, Clark A P, Harris R K, Algaier J W, Smith C S. Comparison of proanthocyanidins in commercial antioxidants: grape seed and pine bark extracts. Journal of Agricultural and Food Chemistry, 2007, 55(1): 148–156

[19] Cadot Y, Miñana-Castelló M T, Chevalier M. Anatomical, histological, and histochemical changes in grape seeds from Vitis vinifera L. cv Cabernet franc during fruit development. Journal of Agricultural and Food Chemistry, 2006, 54(24): 9206–9215

[20] Kennedy J A, Matthews M A, Waterhouse A L. Changes in grape seed polyphenols during fruit ripening. Phytochemistry, 2000, 55(1): 77–85

[21] Kennedy J A, Ristic R, Iland P G, Jones G P, Troup G J, Pilbrow J R, Hutton D R, Hewitt D, Hunter C R. Development of seed polyphenols in berries from Vitis vinifera L. cv. Shiraz. Australian Journal of Grape and Wine Research, 2000, 6(3): 244–254

[22] del Rio J L P, Kennedy J A. Development of proanthocyanidins in Vitis vinifera L. cv. Pinot noir grapes and extraction into wine. American Journal of Enology and Viticulture, 2006, 57(2): 125–132

[23] Moran M A, Sadras V O, Liebich B, Bubner R M. High temp traits differ across varieties. Australian & New Zealand Grapegrower & Winemaker, 2011, 571: 34–35

[24] Cala O, Dufourc E J, Fouquet E, Manigand C, Laguerre M, Pianet I.The colloidal state of tannins impacts the nature of their interaction with proteins: the case of salivary proline-rich protein/procyanidins binding. Langmuir: the ACS Journal of Surfaces and Colloids, 2012, 28(50): 17410–17418

[25] de Freitas V, Mateus N. Structural features of procyanidin interactions with salivary proteins. Journal of Agricultural and Food Chemistry, 2001, 49(2): 940–945

[26] Carvalho E, Mateus N, Plet B, Pianet I, Dufourc E, De Freitas V. Influence of wine pectic polysaccharides on the interactions between condensed tannins and salivary proteins. Journal of Agricultural and Food Chemistry, 2006, 54(23): 8936–8944

[27] Soares S, Mateus N, de Freitas V. Carbohydrates inhibit salivary proteins precipitation by condensed tannins. Journal of Agricultural and Food Chemistry, 2012, 60(15): 3966–3972

[28] Gonçalves R, Mateus N, De Freitas V. Influence of carbohydrates on the interaction of procyanidin B3 with trypsin. Journal of Agricultural and Food Chemistry, 2011, 59(21): 11794–11802

[29] Shirakami Y, Sakai H, Kochi T, Seishima M, Shimizu M. Catechins and its role in chronic diseases. Advances in Experimental Medicine and Biology, 2016, 929: 67–90

[30] Zhang L, Wang Y, Li D, Ho C T, Li J, Wan X. The absorption, distribution, metabolism and excretion of procyanidins. Food & Function, 2016, 7(3): 1273–1281

[31] Glick Z, Joslyn M A. Effect of tannic acid and related compounds on the absorption and utilization of proteins in the rat. Journal of Nutrition, 1970, 100(5): 516–520

[32] Oh H I, Hoff J E. Interaction of condensed grape tannins with pepsin and trypsin in simulated human digestive-system. Nutrition Reports International, 1988, 38(3): 445–453

[33] Bates J M, Akerlund J, Mittge E, Guillemin K. Intestinal alkaline phosphatase detoxifies lipopolysaccharide and prevents inflammation in zebrafish in response to the gut microbiota. Cell Host & Microbe, 2007, 2(6): 371–382

[34] Estaki M, DeCoffe D, Gibson D L. Interplay between intestinal alkaline phosphatase, diet, gut microbes and immunity. World Journal of Gastroenterology, 2014, 20(42): 15650–15656

[35] Malo M S, Alam S N, Mostafa G, Zeller S J, Johnson P V, Mohammad N, Chen K T, Moss A K, Ramasamy S, Faruqui A, Hodin S, Malo P S, Ebrahimi F, Biswas B, Narisawa S, Millán J L, Warren H S, Kaplan J B, Kitts C L, Hohmann E L, Hodin R A. Intestinal alkaline phosphatase preserves the normal homeostasis of gut microbiota. Gut, 2010, 59(11): 1476–1484

[36] Tebib K, Rouanet J M, Besançon P. Effect of grape seed tannins on the activity of some rat intestinal enzyme activities. Enzyme Protein, 1994, 48(1): 51–60

[37] Vallet J, Rouanet J M, Besançon P. Dietary grape seed tannins: effects of nutritional balance and on some enzymic activities along the crypt-villus axis of rat small intestine. Annals of Nutrition & Metabolism, 1994, 38(2): 75–84

[38] Kaliannan K, Hamarneh S R, Economopoulos K P, Nasrin Alam S, Moaven O, Patel P, Malo N S, Ray M, Abtahi S M, Muhammad N, Raychowdhury A, Teshager A, Mohamed M M, Moss A K, Ahmed R, Hakimian S, Narisawa S, Millán J L, Hohmann E, Warren H S, Bhan A K, Malo M S, Hodin R A. Intestinal alkaline phosphatase prevents metabolic syndrome in mice. Proceedings of the National Academy of Sciences of the United States of America, 2013, 110(17): 7003–7008

[39] Sugiyama H, Akazome Y, Shoji T, Yamaguchi A, Yasue M, Kanda T, Ohtake Y. Oligomeric procyanidins in apple polyphenol are main active components for inhibition of pancreatic lipase and triglyceride absorption. Journal of Agricultural and Food Chemistry, 2007, 55(11): 4604–4609

[40] Moreno D A, Ilic N, Poulev A, Brasaemle D L, Fried S K, Raskin I. Inhibitory effects of grape seed extract on lipases. Nutrition, 2003, 19(10): 876–879

[41] Adisakwattana S, Moonrat J, Srichairat S, Chanasit C, Tirapongporn H, Chanathong B, Ngamukote S, Makynen K, Sapwarobol S. Lowering mechanisms of grape seed extract (Vitis vinifera L) and its antihyperlidemic activity. Journal of Medicinal Plants Research, 2010, 4(20): 2113–2120

[42] Donovan J L, Manach C, Rios L, Morand C, Scalbert A, Rémésy C. Procyanidins are not bioavailable in rats fed a single meal containing a grapeseed extract or the procyanidin dimer B3. British Journal of Nutrition, 2002, 87(4): 299–306

[43] Baba S, Osakabe N, Natsume M, Terao J. Absorption and urinary excretion of procyanidin B2 [epicatechin-(4β-8)-epicatechin] in rats. Free Radical Biology & Medicine, 2002, 33(1): 142–148

[44] Choy Y Y, Jaggers G K, Oteiza P I, Waterhouse A L. Bioavailability of intact proanthocyanidins in the rat colon after ingestion of grape seed extract. Journal of Agricultural and Food Chemistry, 2013, 61(1): 121–127

[45] Choy Y Y, Quifer-Rada P, Holstege D M, Frese S A, Calvert C C,Mills D A, Lamuela-Raventos R M, Waterhouse A L.Phenolic metabolites and substantial microbiome changes in pig feces by ingesting grape seed proanthocyanidins. Food & Function, 2014, 5 (9): 2298–2308

[46] Liu W, Zhao S, Wang J, Shi J, Sun Y, Wang W, Ning G, Hong J, Liu R. Molecular Nutrition & Food Research, 2017, 61(9): 1601082

[47] Yokota A, Fukiya S, Islam K B, Ooka T, Ogura Y, Hayashi T, Hagio M, Ishizuka S. Is bile acid a determinant of the gut microbiota on a high-fat diet? Gut Microbes, 2012, 3(5): 455–459

[48] Tamura T, Ozawa M, Tanaka N, Arai S, Mura K. Bacillus cereus response to a proanthocyanidin trimer, a transcriptional and functional analysis. Current Microbiology, 2016, 73(1): 115–123

[49] Tebib K, Bitri L, Besancon P, Rouanet J. Polymeric grape seed tannins prevent plasma cholesterol changes in high-cholesterol-fed rats. Food Chemistry, 1994, 49(4): 403–406

[50] Martin-Carron N, Goni I, Larrauri J A, Garcia-Alonso A, Saura-Calixto F. Reduction in serum total and LDL cholesterol concentrations by a dietary fiber and polyphenol-rich grape product in hypercholesterolemic rats. Nutrition Research, 1999, 19(9): 1371–1381

[51] Nakamura Y, Tonogai Y. Effects of grape seed polyphenols on serum and hepatic lipid contents and fecal steroid excretion in normal and hypercholesterolemic rats. Journal of Health Science, 2002, 48(6): 570–578

[52] Bagchi D, Bagchi M, Stohs S J, Das D K, Ray S D, Kuszynski C A, Joshi S S, Pruess H G. Free radicals and grape seed proanthocyanidin extract: importance in human health and disease prevention. Toxicology, 2000, 148(2–3): 187–197

[53] Bagchi D, Bagchi M, Stohs S, Ray S D, Sen C K, Preuss H G. Cellular protection with proanthocyanidins derived from grape seeds. Annals of the New York Academy of Sciences, 2002, 957(1): 260–270

[54] Bagchi D, Swaroop A, Preuss H G, Bagchi M. Free radical scavenging, antioxidant and cancer chemoprevention by grape seed proanthocyanidin: an overview. Mutation Research, 2014, 768: 69–73

[55] Décordé K, Teissèdre P L, Sutra T, Ventura E, Cristol J P, Rouanet J M. Chardonnay grape seed procyanidin extract supplementation prevents high-fat diet-induced obesity in hamsters by improving adipokine imbalance and oxidative stress markers. Molecular Nutrition & Food Research, 2009, 53(5): 659–666

[56] Zhang Z, Wang H, Jiao R, Peng C, Wong Y M, Yeung V S, Huang Y, Chen Z Y. Choosing hamsters but not rats as a model for studying plasma cholesterol-lowering activity of functional foods. Molecular Nutrition & Food Research, 2009, 53(7): 921–930

[57] Cao H. Adipocytokines in obesity and metabolic disease. Journal of Endocrinology, 2014, 220(2): T47–T59

[58] Andrade-Oliveira V, Camara N O, Moraes-Vieira P M. Adipokines as drug targets in diabetes and underlying disturbances. Journal of Diabetes Research, 2015, 2015: 681612

[59] Jiao R, Zhang Z, Yu H, Huang Y, Chen Z Y. Hypocholesterolemic activity of grape seed proanthocyanidin is mediated by enhancement of bile acid excretion and up-regulation of CYP7A1. Journal of Nutritional Biochemistry, 2010, 21(11): 1134–1139

[60] Bucic-Kojic A, Planinic M, Tomas S, Jakobek L, Seruga M. Influence of solvent and temperature on extraction of phenolic compounds from grape seed, antioxidant activity and colour of extract. International Journal of Food Science & Technology, 2009, 44(12): 2394–2401

[61] Bautista-Ortin A B, Rodriguez-Rodriguez P, Gil-Munoz R, Jimenez-Pascual E, Busse-Valverde N, Martinez-Cutillas A, Lopez-Roca J M, Gomez-Plaza E. Influence of berry ripeness on concentration, qualitative composition and extractability of grape seed tannins. Australian Journal of Grape and Wine Research, 2012, 18(2): 123–130

[62] Cádiz-Gurrea M L, Borrás-Linares I, Lozano-Sánchez J, Joven J, Fernández-Arroyo S, Segura-Carretero A. Cocoa and grape seed byproducts as a source of antioxidant and anti-inflammatory proanthocyanidins. International Journal of Molecular Sciences, 2017, 18(2): E376

[63] Hellström J K, Törrönen A R, Mattila P H. Proanthocyanidins in common food products of plant origin. Journal of Agricultural and Food Chemistry, 2009, 57(17): 7899–7906

[64] Saura-Calixto F. Antioxidant dietary fiber product: a new concept and a potential food ingredient. Journal of Agricultural and Food Chemistry, 1998, 46(10): 4303–4306

[65] Bravo L, Saura-Calixto F. Characterization of dietary fiber and the in vitro indigestible fraction of grape pomace. American Journal of Enology and Viticulture, 1998, 49(2): 135–141

[66] Martin-Carron N, Saura-Calixto F, Goni I. Effects of dietary fibre- and polyphenol-rich grape products on lipidaemia and nutritional parameters in rats. Journal of the Science of Food and Agriculture, 2000, 80(8): 1183–1188

[67] Bravo L, Abia R, Sauracalixto F. Polyphenols as dietary fiber associated compounds—Comparative-study in-vivo and in-vitro properties. Journal of Agricultural and Food Chemistry, 1994, 42(7): 1481–1487

[68] Kim H, Bartley G, Chon J W, Seo K H, Yokoyama W. Chardonnay grape seed flour alters expression of hepatic genes for lipid and glucose metabolism, inflammation, and leptin receptor. FASEB Journal, 2014, 28(1)

[69] Seo K, Kim H, Chon J, Kim D, Nah S, Arvik T, Yokoyama W. Flavonoid-rich Chardonnay grape seed flour supplementation ameliorates diet-induced visceral adiposity, insulin resistance, and glucose intolerance via altered adipose tissue gene expression. Journal of Functional Foods, 2015, 17: 881–891

[70] Kim H, Kim D H, Seo K H, Chon J W, Nah S Y, Bartley G E, Arvik T, Lipson R, Yokoyama W. Modulation of the intestinal microbiota is associated with lower plasma cholesterol and weight gain in hamsters fed Chardonnay grape seed flour. Journal of Agricultural and Food Chemistry, 2015, 63(5): 1460–1467

[71] Li F, Jiang C, Krausz K W, Li Y, Albert I, Hao H, Fabre K M, Mitchell J B, Patterson A D, Gonzalez F J. Microbiome remodelling leads to inhibition of intestinal farnesoid X receptor signalling and decreased obesity. Nature Communications, 2013, 4(1): 2384

[72] Feringa H H, Laskey D A, Dickson J E, Coleman C I. The effect of grape seed extract on cardiovascular risk markers: a meta-analysis of randomized controlled trials. Journal of the American Dietetic Association, 2011, 111(8): 1173–1181

[73] Zhang H, Liu S, Li L, Liu S, Liu S, Mi J, Tian G. The impact of grape seed extract treatment on blood pressure changes: a meta-analysis of 16 randomized controlled trials. Medicine, 2016, 95(33): e4247

Acknowledgements

This work was supported by USDA, ARS CRIS Project 2030-41440-007-00-D.

Compliance with ethics guidelines

Torey Arvik, Hyunsook Kim, James Seiber, and Wallace Yokoyama declare that they have no conflicts of interest or financial conflicts to disclose.

This article is a review and does not contain any studies with human or animal subjects performed by any of the authors.

RIGHTS & PERMISSIONS

The Author(s) 2018. Published by Higher Education Press. This is an open access article under the CC BY license http://creativecommons.org/licenses/by/4.0