Review of Process and Extraction Effects on the Bioavailability of Anthocyanins in Grapes

Year 2024, Volume: 30 Issue: 3, 413 - 423, 23.07.2024

Zehra Gülsünoğlu Konuşkan , Sena Bakır , Tilahun Abera Teka Ayla Elmi Kashtiban Atefeh Karimidastjerd

https://doi.org/10.15832/ankutbd.1326299

Abstract

Grapes are widely consumed worldwide in various forms, including fresh and dried, or processed into products like juice, vinegar, wine, and so on. Anthocyanins, mainly found in grapes, are responsible for various health-promoting effects and contribute to their colours such as red, purple, and blue. Although grapes contain a high quantity of anthocyanins, their bioavailability is considered limited. Anthocyanins may be absorbed by the gastrointestinal wall, undergo intensive first-pass metabolism, and emerge as metabolites in systemic circulation. A significant percentage of some anthocyanins can enter the large intestine and undergo breakdown induced by digestive system microorganisms. Several factors, such as pH, temperature, light, and solvents, can affect anthocyanin bioavailability, and processing grapes into products may impact their bioavailability. Considering the high market share of grapes and grape products, it is important to understand the effects of processing on anthocyanin bioavailability. This review discusses changes in the bioavailability of anthocyanins found in grapes and grape products during food processing, the effect of extraction conditions on bioavailability, as well as the health-promoting effects of grapes and grape products.

Keywords

metabolism, Absorption, Grape products, anthocyanins, Process conditions

References

• Ai J, Wu Q, Battino M, Bai W & Tian L (2021). Using untargeted metabolomics to profile the changes in roselle (Hibiscus sabdariffa L.) anthocyanins during wine fermentation. Food Chemistry 364: 130425
• Aladeboyeje O & Şanli N Ö (2021). Fermented Traditional Probiotic Beverages of Turkish Origin: A Concise Review. International Journal of Life Sciences and Biotechnology 4(3): 546-564
• Alenazi M M, Shafiq M, Alobeed R S, Alsdon A A, Abbasi N A, Ali I & Javed I (2019). Application of abscisic acid at veraison improves red pigmentation and accumulation of dietary antioxidants in red table grapes cv. Red Globe at harvest. Scientia Horticulturae 257: 108672
• Aliakbarlu J, Khalili S, Mohammadi S & Naghili H (2014). Physicochemical properties and antioxidant activity of Doshab (a traditional concen rated grape juice). International Food Research Journal 21: 367–371
• Barba F J, Nikmaram N, Roohinejad S & Khelfa A (2016). Bioavailability of glucosinolates and their breakdown products: Impact of processing. Frontiers in Nutrition 3: 1–35
• Benmeziane F, Cadot Y, Djamai R & Djermoun L (2016). Determination of major anthocyanin pigments and flavonols in red grape skin of some table grape varieties (Vitis vinifera sp.) by high-performance liquid chromatography–photodiode array detection (HPLC-DAD). Oeno One 50: 125–135
• Bi W, Tian M & Row K H (2013). Evaluation of alcohol-based deep eutectic solvent in extraction and determination of flavonoids with response surface methodology optimization. Journal of Chromatography A 1285: 22–30
• Bitsch R, Netzel M, Frank T, Strass G & Bitsch I (2004). Bioavailability and biokinetics of anthocyanins from red grape juice and red wine. Journal of Biomedicine and Biotechnology 4: 293–298
• Bonfigli M, Godoy E, Reinheimer M A & Scenna N J (2017). Comparison between conventional and ultrasound-assisted techniques for extraction of anthocyanins from grape pomace. Experimental results and mathematical modeling. Journal of Food Engineering 207: 56–72
• Bosiljkov T, Dujmić F, Cvjetko Bubalo M, Hribar J, Vidrih R, Brnčić M, Zlatic E, Redovnikovic I R & Jokic S (2017). Natural deep eutectic solvents and ultrasound-assisted extraction: Green approaches for extraction of wine lees anthocyanins. Food and Bioproducts Processing 102: 195–203
• Bozkurt H, Gögüş F & Eren S (1999). Nonenzymic browning reactions in boiled grape juice and its models during storage. Food Chemistry 64: 89–93
• Bub A, Watzl B, Heeb D, Rechkemmer G & Briviba K (2001). Malvidin-3-glucoside bioavailability in humans after ingestion of red wine, dealcoholized red wine and red grape juice. European Journal of Nutrition 40: 113–120
• Busse-valverde N, Encarna G, Jose M L & Bautista-ortín A B (2011). The Extraction of Anthocyanins and Proanthocyanidins from Grapes to Wine during Fermentative Maceration Is Affected by the Enological Technique. Journal of Agricultural and Food Chemistry 59: 5450–5455
• Cahyana Y, Gordon M H & Gibson T M (2019). Urinary Excretion of Anthocyanins following Consumption of Strawberry and Red Grape Juice. International Journal for Vitamin and Nutrition Research 89: 29–36
• Castello F, Costabile G, Bresciani L, Tassotti M, Naviglio D, Luongo D, Ciciola P, Vitale M, Vetrani C, Galaverna G, Brighenti F, Giacco R, Del rio D & Mena P (2018). Bioavailability and pharmacokinetic profile of grape pomace phenolic compounds in humans. Archives of Biochemistry and Biophysics 646: 1–9
• de Castilhos M B M, Corrêa O L dos S, Zanus M C, Maia J D G, Gómez-Alonso S & García-Romero E (2015). Pre-drying and submerged cap winemaking: Effects on polyphenolic compounds and sensory descriptors. Part II: BRS Carmem and Bordô (Vitis labrusca L.). Food Research International 76: 697–708
• Celli G B & Brooks M S (2017). Impact of extraction and processing conditions on betalains and comparison of properties with anthocyanins — A current review. Food Research International 100: 501–509
• Cheynier V, Gomez C & Ageorges A (2012). Flavonoids: Anthocyanins. In: M L Leo & F T Nollet (Eds.), Handbook of Analysis of Active Compounds in Functional Foods, CRC Press pp. 379–403
• Copetti C, Franco F W, Machado E D R, Soquetta M B, Quatrin A, Ramos V D M & Penna N G (2018). Acute consumption of bordo grape juice and wine improves serum antioxidant status in healthy individuals and inhibits reactive oxygen species production in human neuron-like cells. Journal of Nutrition and Metabolism pp. 1–11
• Corrales M, García A F, Butz P & Tauscher B (2009) Extraction of anthocyanins from grape skins assisted by high hydrostatic pressure. Journal of Food Engineering 90: 415–421
• Cosme F, Pinto T & Vilela A (2018). Phenolic Compounds and Antioxidant Activity in Grape Juices: A Chemical and Sensory View. Beverages 4: 22
• Crozier A, Jaganath I B, Clifford M N (2009). Dietary phenolics: Chemistry, bioavailability and effects on health. Natural Products Reports, 26(8): 1001-1043. https://doi.org/10.1039/b802662a.
• Cvjetko Bubalo M, Ćurko N, Tomašević M, Kovačević Ganić K & Radojcic Redovnikovic I (2016). Green extraction of grape skin phenolics by using deep eutectic solvents. Food Chemistry 200: 159–166
• De Rosso M, Tonidandel L, Larcher R, Nicolini G, Ruggeri V, Dalla Vedova A (2012). Study of anthocyanic profiles of twenty-one hybrid grape varieties by liquid chromatography and precursor-ion mass spectrometry. Analytica Chimica Acta 732: 120–129
• Drosou C, Kyriakopoulou K, Bimpilas A, Tsimogiannis D, Krokida M (2015). A comparative study on different extraction techniques to recover red grape pomace polyphenols from vinification byproducts. Ind Crops Prod 75: 141–149
• Eker M E, Aaby K, Budic-Leto I, Rimac S, Brnči´c B, Nehir El S (2019). A review of factors affecting anthocyanin bioavailability: Possible implications for the inter-individual variability. Foods 9(1): 2
• Elmi Kashtiban A & Esmaiili M (2019). Extraction of phenolic compounds from Siah-Sardasht grape skin using subcritical water and ultrasound pretreatment. Journal of Food Processing and Preservation 43: 1–10
• Enaru B, Drețcanu G, Pop T D, Stǎnilǎ A & Diaconeasa Z (2021). Anthocyanins: Factors Affecting Their Stability and Degradation. Antioxidants 10: 1967
• Esclapez M D, García-Pérez J V, Mulet A & Cárcel J A (2011). Ultrasound-Assisted Extraction of Natural Products. Food Engineering Reviews 3: 108–120
• Fang J (2014). Bioavailability of anthocyanins. Drug Metabolism Reviews 46(4): 508–520. https://doi.org/10.3109/03602532.2014.978080
• Fang J (2015). Classification of fruits based on anthocyanin types and relevance to their health effects. Nutrition 31: 1301–1306
• FAO. FAOSTAT online database. FAOSTAT Online Database 2021. https://www.fao.org/faostat/en/#data/QCL (accessed December 22, 2023).
• Faria A, Pestana D, Azevedo J, Martel F, de Freitas V & Azevedo I (2009). Absorption of anthocyanins through intestinal epithelial cells—Putative involvement of GLUT2. Molecular Nutrition and Food Research 53: 1430–1437
• FDA (Food and Drug Administration). Title 21 Code of Federal Regulations (CFR) Part 320. National Archives and Records Administration, USA. 2001
• Fernandes I, Faria A, de Freitas V, Calhau C, Mateus N (2015). Multiple-approach studies to assess anthocyanin bioavailability. Phytochemistry Reviews 14: 899–919
• Fernandes I, Marques C, Évora A, Cruz L, de Freitas V, Calhau C, Faria A & Mateus N (2017). Pharmacokinetics of Table and Port Red Wine Anthocyanins: A Crossover Trial in Healthy Men. Food and Function 8(5): 2030–2037
• Fernandes I, Marques C, Évora A, Faria A, Calhau C, Mateus N & de Freitas V (2019). Anthocyanins: Nutrition and Health. In: J M Merillon & K G Ramawat (Eds.), Bioactive molecules in food, Springer Cham, Switzerland AG pp. 1097-1133
• Fernandes I, Nave F, Gonçalves R, de Freitas V & Mateus N (2012). On the bioavailability of flavanols and anthocyanins: Flavanol–anthocyanin dimers. Food Chemistry 135: 812–818
• Fernández-García E, Carvajal-Lérida I & Pérez-Gálvez A (2009). In vitro bioaccessibility assessment as a prediction tool of nutritional efficiency. Nutrition Research 29: 751–760
• Fleschhut J, Kratzer F, Rechkemmer G & Kulling S E (2006). Stability and biotransformation of various dietary anthocyanins in vitro. European Journal of Nutrition 45: 7–18
• Frank T, Netzel M, Strass G, Bitsch R & Bitsch I (2003). Bioavailability of Anthocyanidin-3-Glucosides Following Consumption of Red Wine and Red Grape Juice. Canadian Journal of Physiology and Pharmacology 81(5): 423–435. doi:10.1139/y03-038
• Gulsunoglu-Konuskan Z & Kilic-Akyilmaz M (2021). Microbial Bioconversion of Phenolic Compounds in Agro-industrial Wastes: A Review of Mechanisms and Effective Factors. Journal of Agricultural and Food Chemistry 70(23): 6901-6910
• Han F, Yang P, Wang H, Fernandes I, Mateus N & Liu Y (2019). Digestion and absorption of red grape and wine anthocyanins through the gastrointestinal tract. Trends in Food Science and Technology 83: 211–224 He F, Mu L, Yan G L, Liang N N, Pan Q H, Wang J, Reeves M J & Duan C Q (2010). Biosynthesis of anthocyanins and their regulation in colored grapes. Molecules 15: 9057–9091
• He J, Magnuson B A, Lala G, Tian Q, Schwartz S J & Giusti M M (2006). Intact Anthocyanins and Metabolites in Rat Urine and Plasma After 3 Months of Anthocyanin Supplementation. Nutrition and Cancer 54: 3–12
• Henriques J F, Serra D, Dinis T C P & Almeida L M (2020). The Anti-Neuroinflammatory Role of Anthocyanins and Their Metabolites for the Prevention and Treatment of Brain Disorders. International Journal of Molecular Sciences 21(22): 1-31
• Hornedo-Ortega R, Rasines-Perea Z, Jourdes A B C, Teissedre P L, Jourdes M (2021). Anthocyanins: Dietary Sources, Bioavailability, Human Metabolic Pathways, and Potential Anti-Neuroinflammatory Activity. OpenIntech.
• Iannone A, Sapone V, Di L, Cicci A (2021). Extraction of Anthocyanins from Grape (Vitis vinifera) Skins Employing Natural Deep Eutectic Solvents (NaDES). Chemical Engineering Transactions 87: 469–474
• Iglesias-Carres L, Mas-Capdevila A, Bravo FI, Aragonès G, Arola-Arnal A & Muguerza B (2019). A comparative study on the bioavailability of phenolic compounds from organic and nonorganic red grapes. Food Chemistry 30(299): 125092
• Ioannou I, Hafsa I, Hamdi S, Charbonnel C & Ghoul M (2012). Review of the effects of food processing and formulation on flavonol and anthocyanin behaviour. Journal of Food Engineering 111: 208–217
• Jankowski A, Jankowska B & Niedworok J (2000). The effects of anthocyanin dye from grapes on experimental diabetes. Folia Medica Cracoviensia 41: 5–15
• Jeszka-skowron M & Czarczyńska-Goślińska B (2020). Raisins and the other dried fruits : Chemical profile and health benefits. The Mediterranean Diet pp. 229–238
• Ju Z & Howard LR (2005). Subcritical water and sulfured water extraction of anthocyanins and other phenolics from dried red grape skin. Journal of Food Science 70: 270–276
• Kamiloglu S, Capanoglu E, Grootaert C & Camp J Van (2015). Anthocyanin Absorption and Metabolism by Human Intestinal Caco-2 Cells — A Review. International Journal of Molecular Sciences 16(9): 21555–21574 Kaya S & Maskan A (2003). Water vapor permeability of pestil (a fruit leather) made from boiled grape juice with starch. Journal of Food Engineering 57: 295–299
• Kuntz S, Rudloff S, Asseburg H, Borsch C, Frohling B, Unger F, Dold S, Spengler B, Römpp A & Kunz C (2015). Uptake and bioavailability of anthocyanins and phenolic acids from grape / blueberry juice and smoothie in vitro and in vivo. British Journal of Nutrition 113(7): 1044-1055
• Lapornik B, Prošek M & Wondra AG (2005). Comparison of extracts prepared from plant by-products using different solvents and extraction time. Journal of Food Engineering 71: 214–222
• Lee Y-M, Yoom Y, Yoon H & Song S (2017). Dietary Anthocyanins against Obesity and Inflammation. Nutrients 9: 1–15
• Leong S Y & Oey I (2012) Effects of processing on anthocyanins, carotenoids and vitamin C in summer fruits and vegetables. Food Chemistry 133: 1577–1587
• Lingua M S, Wunderlin D A & Baroni M V (2018). Effect of Simulated Digestion on the Phenolic Components of Red Grapes and Their Corresponding Wines. Journal of Functional Foods 44: 86–94
• Liu Q, Tang G Y, Zhao C N, Feng X L, Xu X Y & Cao S Y (2018). Comparison of antioxidant activities of different grape varieties. Molecules 23: 1–17
• Luque-Rodríguez J M, Luque de Castro M D & Pérez-Juan P (2007). Dynamic superheated liquid extraction of anthocyanins and other phenolics from red grape skins of winemaking residues. Bioresource Technology 98: 2705–2713
• Makris D P, Boskou G, Chiou A & Andrikopoulos N K (2008). An investigation on factors affecting recovery of antioxidant phenolics and anthocyanins from red grape (Vitis vinifera L.) pomace employing water/ethanol-based solutions. American Journal of Food Technology 3: 164–173
• Mandal V, Mohan Y, Hemalatha S (2007). Microwave Assisted Extraction – An Innovative and Promising Extraction Tool for Medicinal Plant Research. Pharmacognosy Reviews 1(1): 7-18
• Mattioli R, Francioso A, Mosca L & Silva P (2020). Anthocyanins : A Comprehensive Review of Their Chemical Properties and Health Effects on Cardiovascular and Neurodegenerative Diseases. Molecules 25: 1–42
• McDougall G J, Dobson P, Smith P, Blake A & Stewart D (2005). Assessing potential bioavailability of raspberry anthocyanins using an in vitro digestion system. Journal of Agricultural and Food Chemistry 53: 5896–5904
• Monrad J K, Howard L R, King J W, Srinivas K & Mauromoustakos A (2010). Subcritical solvent extraction of anthocyanins from dried red grape pomace. Journal of Agricultural and Food Chemistry 58: 2862–2868
• Morata A, Escott C, Loira I, Carmen L, Palomero F & Gonz C (2021). Emerging Non-Thermal Technologies for the Extraction of Grape Anthocyanins. Antioxidants 10(12): 1863
• Murkovic M, Mülleder U, Adam U & Pfannhauser W (2001). Detection of anthocyanins from elderberry juice in human urine. Journal of the Science of Food and Agriculture 81: 934–937
• Oh Y S, Lee J H, Yoon S H, Oh C H, Choi D S, Choe E & Jung M Y (2008). Characterization and quantification of anthocyanins in grape juices obtained from the grapes cultivated in Korea by HPLC/DAD, HPLC/MS, and HPLC/MS/MS. Journal of Food Science 73: 378–389
• Olivati C, Paula Y, Nishiyama D O, Souza T De, Janzantti N S, Aparecida M, Gomes E, Hermosin-Gutierrez I, Silva R & Lago-Vansela E S (2019). Effect of the pre-treatment and the drying process on the phenolic composition of raisins produced with a seedless Brazilian grape cultivar. Food Research International 116: 190–199
• Oliveira H, Perez-Gregório R, de Freitas V, Mateus N, Fernandes I (2019). Comparison of the in vitro gastrointestinal bioavailability of acylated and non-acylated anthocyanins: Purple-fleshed sweet potato vs red wine. Food Chemistry 276: 410–418
• Overall J, Bonney S, Wilson M, Beermann A, Grace M, Esposito D, Lila M A & Komarnytsky S (2017). Metabolic Effects of Berries with Structurally Diverse Anthocyanins. International Journal of Molecular Sciences 18: 422 Ozturk B & Anli E (2014). Different techniques for reducing alcohol levels in wine : A review. BIO Web of Conferences 3: 2–9
• Pacheco S M, Soares M S P, Gutierres J M, Gerzson M F B, Carvalho F B, Azambuja J H, Schetinger M R C, Stefanello F M & Spanevello R M (2018). Anthocyanins as a Potential Pharmacological Agent to Manage Memory Deficit, Oxidative Stress and Alterations in Ion Pump Activity Induced by Experimental Sporadic Dementia of Alzheimer’s Type. The Journal of Nutritional Biochemistry 56: 193–204
• Panić M, Gunjević V, Cravotto G & Redovnikovic I R (2019). Enabling technologies for the extraction of grape-pomace anthocyanins using natural deep eutectic solvents in up-to-half-litre batches extraction of grape pomace anthocyanins using NADES. Food Chemistry 300: 125185
• Passamonti S, Vrhovsek U, Vanzo A & Mattivi F (2005). Fast access of some grape pigments to the brain. Journal of Agricultural and Food Chemistry 53: 7029–7034
• Patras A, Brunton NP, O’Donnell C & Tiwari BK (2010). Effect of thermal processing on anthocyanin stability in foods; mechanisms and kinetics of degradation. Trends in Food Science and Technology 21: 3–11
• Pineda-Vadillo C, Nau F, Guerin-Dubiard C, Jardin J, Lechevalier V, Sanz-Buenhombre M, Guadarrama A, Toth T, Csavajda E, Hingyi H, Karakaya S, Sibakov J, Capozzi F, Bordoni A & Dupont D (2017). The food matrix affects the anthocyanin profile of fortified egg and dairy matrices during processing and in vitro digestion. Food Chemistry 214: 486–496
• Polia F, Pastor-belda M, Mart A, Horcajada M & Tom F A (2022). Technological and Biotechnological Processes to Enhance the Bioavailability of Dietary (Poly)phenols in Humans. Journal of Agricultural and Food Chemistry 70(7): 2092–2107
• Pomar F, Novo M & Masa A (2005). Varietal differences among the anthocyanin profiles of 50 red table grape cultivars studied by high performance liquid chromatography. Journal of Chromatography A 1094: 34-41
• Revilla E, Ryan J M & Martín-Ortega G (1998). Comparison of Several Procedures Used for the Extraction of Anthocyanins from Red Grapes. Journal of Agricultural and Food Chemistry 46: 4592–4597
• Romero-Cascales I, Fernandez-Fernandez J I, Lopez-Roca J M & Gomez-Plaza E (2005). The maceration process during winemaking extraction of anthocyanins from grape skins into wine. European Food Research and Technology 221: 163–167
• Ruta L L & Farcasanu I C (2019). Anthocyanins and Anthocyanin-Derived Products in. Antioxidants 8: 1–13 Sabra A, Netticadan T & Wijekoon C (2021). Grape bioactive molecules and the potential health benefits in reducing the risk of heart diseases. Food Chemistry X:100149
• Seymour E M, Tanone I I, Urcuyo-Llanes D E, Lewis S K, Kirakosyan A & Kondoleon M G (2011). Blueberry intake alters skeletal muscle and adipose tissue peroxisome proliferator-activated receptor activity and reduces insulin resistance in obese rats. Journal of Medicinal Food 14: 1511–1518
• Seymour E M, Wolforth J, Bosak K, Kondoleon M, Mehta V & Brickner P (2013). Effect of tart cherry versus PPAR agonist pioglitazone on stroke-related phenotypes and inflammation. The FASEB Journal 27: 7
• Soares S, Garcia-Estévez I, Ferrer-Galego R, Brás NF, Brandão E, Silva M, et al. (2018). Study of human salivary proline-rich proteins interaction with food tannins. Food Chemistry 243:175-185
• Spigno G, Tramelli L & De Faveri D M (2007). Effects of extraction time, temperature and solvent on concentration and antioxidant activity of grape marc phenolics. Journal of Food Engineering 81: 200–208
• Stalmach A, Edwards C A, Wightman J D & Crozier A (2012). Gastrointestinal stability and bioavailability of (poly)phenolic compounds following ingestion of Concord grape juice by humans. Molecular Nutrition and Food Research 56: 497–509
• Tagliazucchi D, Verzelloni E, Helal A & Conte A (2013). Effect of grape variety on the evolution of sugars, hydroxymethylfurfural, polyphenols and antioxidant activity during grape must cooking. International Journal of Food Science and Technology 48: 808–816
• Tena N & Asuero A G (2022). Up-To-Date Analysis of the Extraction Methods for Anthocyanins: Principles of the Techniques, Optimization, Technical Progress, and Industrial Application. Antioxidants 11(2): 286
• Vergara-salinas J R, Bulnes P, Agosin E & Pe J R (2013). Effect of Pressurized Hot Water Extraction on Antioxidants from Grape Pomace before and after enological fermentation. Journal of Agricultural Food and Chemistry 61(28): 6929–6936
• Waterhouse A L (2002). Wine phenolics. Annals of the New York Academy of Sciences 957(1): 21–36 Weber F & Larsen L R (2017). Influence of fruit juice processing on anthocyanin stability. Food Research International 100: 354–365
• Yamakoshi J, Kataoka S, Koga T & Ariga T (1999). Proanthocyanidin-rich extract from grape seeds attenuates the development of aortic atherosclerosis in cholesterol-fed rabbits. Atherosclerosis 142: 139–149
• Yang P, Yuan C, Wang H, Han F, Liu Y, Wang L & Liu Y (2018). Stability of Anthocyanins and Their Degradation Products from Cabernet Sauvignon Red Wine under Gastrointestinal pH and Temperature Conditions. Molecules 23: 354
• Yuzuak S & Xie D (2022). Anthocyanins from muscadine (Vitis rotundifolia) grape fruit. Current Plant Biology 30: 100243