Phytochemical Composition, Antioxidant and Antiproliferative Activities of Defatted Sea Buckthorn (Hippophaë rhamnoides L.) Berry Pomace Fractions Consecutively Recovered by Pressurized Ethanol and Water

This study aimed at valorisation of sea buckthorn pomace (SBP) for the production of extracts containing valuable bioactive compounds. For this purpose, SBP defatted by supercritical CO2 was subjected to consecutive fractionation with pressurized ethanol and water, which yielded 11.9% and 4.8% of extracts, respectively. The extracts were evaluated for their antioxidant potential, phytochemical composition and antiproliferative effects against cancer cells. Water extracts exhibited remarkably higher values in Folin-Ciocalteu assay of total phenolic content, oxygen radical absorbance capacity (ORAC), ABTS●+/DPPH● scavenging and cellular antioxidant activity (CAA) assays and more efficiently inhibited proliferation of HT29 cells at non-cytotoxic concentrations measured in non-tumoral Caco2 cells. Among 28 detected and 21 quantified phytochemicals, flavonols with the structures of isorhamnetin (five compounds), quercetin (three compounds), kaempferol (three compounds) glycosides and catechin (six compounds) were the most abundant in the extracts. In conclusion, the applied method of fractionation of SBP produces promising natural antioxidant complexes with antiproliferative properties that could find potential applications in nutraceuticals, functional foods and cosmeceuticals.

[1]  N. Seeram.  BERRIES , 2022, Becoming Rooted.

[2]  Ł. Bobak,et al.  Anti-Oxidant and Anti-Enzymatic Activities of Sea Buckthorn (Hippophaë rhamnoides L.) Fruits Modulated by Chemical Components , 2019, Antioxidants.

[3]  A. Cifuentes,et al.  Polymethoxylated Flavones Target Cancer Stemness and Improve the Antiproliferative Effect of 5-Fluorouracil in a 3D Cell Model of Colorectal Cancer , 2019, Nutrients.

[4]  D. Mcclements,et al.  Comparison of phytochemical profiles and antiproliferative activities of different proanthocyanidins fractions from Choerospondias axillaris fruit peels. , 2018, Food research international.

[5]  G. Goel,et al.  Influence of polyphenol rich seabuckthorn berries juice on release of polyphenols and colonic microbiota on exposure to simulated human digestion model. , 2018, Food research international.

[6]  E. Sugano,et al.  Comparison of neuroprotective effects of oil- and water-soluble fractions of sea buckthorn juice against light-induced retinal degeneration in rats , 2018 .

[7]  P. Venskutonis,et al.  Valorization of six Nepeta species by assessing the antioxidant potential, phytochemical composition and bioactivity of their extracts in cell cultures , 2018, Journal of Functional Foods.

[8]  B. Olas,et al.  The Anticancer Activity of Sea Buckthorn [Elaeagnus rhamnoides (L.) A. Nelson] , 2018, Front. Pharmacol..

[9]  Gitishree Das,et al.  A critical analysis of extraction techniques used for botanicals: Trends, priorities, industrial uses and optimization strategies , 2018 .

[10]  P. Alves,et al.  Polymethoxylated Flavones from Orange Peels Inhibit Cell Proliferation in a 3D Cell Model of Human Colorectal Cancer , 2018, Nutrition and cancer.

[11]  R. Liu,et al.  Phenolic compounds, antioxidant activity, antiproliferative activity and bioaccessibility of Sea buckthorn (Hippophaë rhamnoides L.) berries as affected by in vitro digestion. , 2017, Food & function.

[12]  P. Venskutonis,et al.  Fractionation of sea buckthorn pomace and seeds into valuable components by using high pressure and enzyme-assisted extraction methods , 2017 .

[13]  X. Zhai,et al.  Chemical fingerprint and quantitative analysis of flavonoids for quality control of Sea buckthorn leaves by HPLC and UHPLC-ESI-QTOF-MS , 2017 .

[14]  M. Tobiszewski,et al.  Extraction with environmentally friendly solvents , 2017 .

[15]  P. Venskutonis,et al.  Biorefining of blackcurrant pomace into high value functional ingredients using supercritical CO2, pressurized liquid and enzyme assisted extractions , 2017 .

[16]  R. Liu,et al.  Comparative assessment of phytochemical profiles, antioxidant and antiproliferative activities of Sea buckthorn (Hippophaë rhamnoides L.) berries. , 2017, Food chemistry.

[17]  Baoru Yang,et al.  Phenolic compounds extracted by acidic aqueous ethanol from berries and leaves of different berry plants. , 2017, Food chemistry.

[18]  M. Kowalczyk,et al.  Tentative Characterization of Polyphenolic Compounds in the Male Flowers of Phoenix dactylifera by Liquid Chromatography Coupled with Mass Spectrometry and DFT , 2017, International journal of molecular sciences.

[19]  H. Lee,et al.  Sea Buckthorn Leaf Extract Inhibits Glioma Cell Growth by Reducing Reactive Oxygen Species and Promoting Apoptosis , 2017, Applied Biochemistry and Biotechnology.

[20]  N. Pavlović,et al.  Supercritical CO2 extraction of sea buckthorn , 2016 .

[21]  O. Laaksonen,et al.  Flavonol glycosides in berries of two major subspecies of sea buckthorn (Hippophaë rhamnoides L.) and influence of growth sites. , 2016, Food chemistry.

[22]  P. Venskutonis,et al.  Fractionation of black chokeberry pomace into functional ingredients using high pressure extraction methods and evaluation of their antioxidant capacity and chemical composition , 2016 .

[23]  P. Górnaś,et al.  Seeds recovered from industry by-products of nine fruit species with a high potential utility as a source of unconventional oil for biodiesel and cosmetic and pharmaceutical sectors. , 2016 .

[24]  P. Venskutonis,et al.  Optimization of high pressure extraction processes for the separation of raspberry pomace into lipophilic and hydrophilic fractions , 2016 .

[25]  Yongkyu Lee,et al.  Cancer Chemopreventive Potential of Procyanidin , 2015, Toxicological research.

[26]  P. Górnaś,et al.  Seed oils recovered from industrial fruit by-products are a rich source of tocopherols and tocotrienols: Rapid separation of α/β/γ/δ homologues by RP-HPLC/FLD , 2015 .

[27]  S. Graziano,et al.  Evaluation of the antioxidant activity of foods in human cells , 2015 .

[28]  A. Wojdyło,et al.  Analysis of Lipophilic and Hydrophilic Bioactive Compounds Content in Sea Buckthorn (Hippophaë rhamnoides L.) Berries. , 2015, Journal of agricultural and food chemistry.

[29]  Li-Ming Zhou,et al.  Anti-proliferation effects of isorhamnetin on lung cancer cells in vitro and in vivo. , 2015, Asian Pacific journal of cancer prevention : APJCP.

[30]  G. Nuernberg,et al.  Sea buckthorn pomace supplementation in the finishing diets of pigs – are there effects on meat quality and muscle fatty acids? , 2015 .

[31]  Richard G. Moore,et al.  The cranberry flavonoids PAC DP-9 and quercetin aglycone induce cytotoxicity and cell cycle arrest and increase cisplatin sensitivity in ovarian cancer cells , 2015, International journal of oncology.

[32]  Hélder D. Silva,et al.  Edible Bio-Based Nanostructures: Delivery, Absorption and Potential Toxicity , 2015, Food Engineering Reviews.

[33]  S. Tuleukhanov,et al.  Antitumor Activity of Ethanol Extract from Hippophae Rhamnoides L. Leaves towards Human Acute Myeloid Leukemia Cells In Vitro , 2014, Bulletin of Experimental Biology and Medicine.

[34]  Baoru Yang,et al.  Proanthocyanidins in wild sea buckthorn (Hippophaë rhamnoides) berries analyzed by reversed-phase, normal-phase, and hydrophilic interaction liquid chromatography with UV and MS detection. , 2014, Journal of agricultural and food chemistry.

[35]  J. Ouyang,et al.  Inhibitory effects of sea buckthorn procyanidins on fatty acid synthase and MDA-MB-231 cells , 2014, Tumor Biology.

[36]  S. Bastian,et al.  Low Molecular Weight Procyanidins from Grape Seeds Enhance the Impact of 5-Fluorouracil Chemotherapy on Caco-2 Human Colon Cancer Cells , 2014, PloS one.

[37]  P. Górnaś,et al.  Seeds recovered from by-products of selected fruit processing as a rich source of tocochromanols: RP-HPLC/FLD and RP-UPLC-ESI/MSn study , 2014, European Food Research and Technology.

[38]  Haidy A. Gad,et al.  Metabolomics driven analysis of six Nigella species seeds via UPLC-qTOF-MS and GC-MS coupled to chemometrics. , 2014, Food chemistry.

[39]  C. Santos-Buelga,et al.  Anti-proliferative effects of quercetin and catechin metabolites. , 2014, Food & function.

[40]  L. Gu,et al.  Absorption and metabolism of proanthocyanidins , 2014 .

[41]  Junbo Hu,et al.  Isorhamnetin suppresses colon cancer cell growth through the PI3K‑Akt‑mTOR pathway. , 2014, Molecular medicine reports.

[42]  T. Stobdan,et al.  Nutritional Attributes and Health Application of Seabuckthorn ( Hippophae rhamnoides L.) – A Review , 2013 .

[43]  R. Liu.  Health-promoting components of fruits and vegetables in the diet. , 2013, Advances in nutrition.

[44]  A. Denicola,et al.  Evaluating the antioxidant capacity of natural products: a review on chemical and cellular-based assays. , 2013, Analytica chimica acta.

[45]  Sung-Hoon Kim,et al.  Tanshinones: Sources, Pharmacokinetics and Anti-Cancer Activities , 2012, International journal of molecular sciences.

[46]  T. Choshi,et al.  Influence of gallate and pyrogallol moieties on the intestinal absorption of (-)-epicatechin and (-)-epicatechin gallate. , 2012, Journal of food science.

[47]  C. Arumughan,et al.  HPLC-DAD-MS/MS profiling of antioxidant flavonoid glycosides in sea buckthorn (Hippophae rhamnoides L.) seeds , 2012, International journal of food sciences and nutrition.

[48]  E. Christaki.  Hippophae Rhamnoides L. (Sea Buckthorn): a Potential Source of Nutraceuticals , 2012 .

[49]  V. Kant,et al.  Total phenolic contents and free radical scavenging activities of different extracts of seabuckthorn (Hippophae rhamnoides) pomace without seeds , 2012, International journal of food sciences and nutrition.

[50]  M. Bizzarri,et al.  Antiproliferative and Apoptotic Effects Triggered by Grape Seed Extract (GSE) versus Epigallocatechin and Procyanidins on Colon Cancer Cell Lines , 2012, International journal of molecular sciences.

[51]  Pragya Sharma,et al.  Nutritional and antimicrobial property of seabuckthorn ( Hippophae sp.) seed oil , 2011 .

[52]  Asheesh Gupta,et al.  Medicinal and therapeutic potential of Sea buckthorn (Hippophae rhamnoides L.). , 2011, Journal of ethnopharmacology.

[53]  Venkatesh Meda,et al.  Sea buckthorn berries: A potential source of valuable nutrients for nutraceuticals and cosmoceuticals , 2011 .

[54]  F. Chemat,et al.  Solvent Free Microwave-Assisted Extraction of Antioxidants from Sea Buckthorn (Hippophae rhamnoides) Food By-Products , 2011 .

[55]  I. Goñi,et al.  The contribution of fruits and vegetables to dietary intake of polyphenols and antioxidant capacity in a Mexican rural diet: Importance of fruit and vegetable variety , 2011 .

[56]  Yizhou Dong,et al.  Biosynthesis, total syntheses, and antitumor activity of tanshinones and their analogs as potential therapeutic agents. , 2011, Natural product reports.

[57]  P. Adlercreutz,et al.  Antiproliferative effects of sea buckthorn (Hippophae rhamnoides L.) extracts on human colon and liver cancer cell lines , 2010 .

[58]  Baoru Yang,et al.  Flavonol glycosides in wild and cultivated berries of three major subspecies of Hippophaë rhamnoides and changes during harvesting period , 2009 .

[59]  Kumiko Goto,et al.  Anti-tumor promoters phenolics and triterpenoid from Hippophae rhamnoides. , 2009, Fitoterapia.

[60]  S. Katiyar,et al.  Multi-targeted prevention and therapy of cancer by proanthocyanidins. , 2008, Cancer letters.

[61]  R. Liu,et al.  Cellular antioxidant activity of common fruits. , 2008, Journal of agricultural and food chemistry.

[62]  H. Ross,et al.  Berry extracts exert different antiproliferative effects against cervical and colon cancer cells grown in vitro. , 2008, Journal of agricultural and food chemistry.

[63]  Rui Hai Liu,et al.  Cellular antioxidant activity (CAA) assay for assessing antioxidants, foods, and dietary supplements. , 2007, Journal of agricultural and food chemistry.

[64]  H. Kallio,et al.  Quality components of sea buckthorn (Hippophae rhamnoides) varieties. , 2005, Journal of agricultural and food chemistry.

[65]  M. Gul,et al.  Hippophae rhamnoides L.: chromatographic methods to determine chemical composition, use in traditional medicine and pharmacological effects. , 2004, Journal of chromatography. B, Analytical technologies in the biomedical and life sciences.

[66]  M. Don,et al.  Antitumor Agents. 239. Isolation, structure elucidation, total synthesis, and anti-breast cancer activity of neo-tanshinlactone from Salvia miltiorrhiza. , 2004, Journal of medicinal chemistry.

[67]  A. Krumbein,et al.  Antioxidant gallocatechins, dimeric and trimeric proanthocyanidins from sea buckthorn (Hippophaë rhamnoides) pomace , 2004 .

[68]  A. Krumbein,et al.  Structural investigations of flavonol glycosides from sea buckthorn (Hippophaë rhamnoides) pomace by NMR spectroscopy and HPLC-ESI-MS(n). , 2004, Journal of agricultural and food chemistry.

[69]  D. Knorr,et al.  Structure-antioxidant efficiency relationships of phenolic compounds and their contribution to the antioxidant activity of sea buckthorn juice. , 2003, Journal of agricultural and food chemistry.

[70]  F. Tomás-Barberán,et al.  HPLC-DAD-MS/MS ESI characterization of unusual highly glycosylated acylated flavonoids from cauliflower (Brassica oleracea L. var. botrytis) agroindustrial byproducts. , 2003, Journal of agricultural and food chemistry.

[71]  Dejian Huang,et al.  Development and validation of oxygen radical absorbance capacity assay for lipophilic antioxidants using randomly methylated beta-cyclodextrin as the solubility enhancer. , 2002, Journal of agricultural and food chemistry.

[72]  Baoru Yang,et al.  Fatty acid composition of lipids in sea buckthorn (Hippophaë rhamnoides L.) berries of different origins. , 2001, Journal of agricultural and food chemistry.

[73]  W. Friedrich,et al.  Investigation of proanthocyanidins by HPLC with electrospray ionization mass spectrometry , 2000 .

[74]  T. Beveridge,et al.  Sea buckthorn products: manufacture and composition. , 1999, Journal of agricultural and food chemistry.

[75]  P. Pellett.  Food and agricultural organization of the United Nations : Technical report , 1996 .

[76]  P. Venskutonis,et al.  Modeling and optimization of supercritical carbon dioxide extraction for isolation of valuable lipophilic constituents from elderberry (Sambucus nigra L.) pomace , 2020 .

[77]  Valorization of Fruit Processing By-products , 2020 .

[78]  J. Blaha,et al.  THE EFFECT OF SEA BUCKTHORN (HIPPOPHAE RHAMNOIDES L.) RESIDUES IN COMPOUND FEEDS ON THE PERFORMANCE AND SKIN COLOR OF BROILERS , 2014 .

[79]  J. Gustavsson.  Global food losses and food waste , 2011 .

[80]  Kenneth Helrick,et al.  Official methods of analysis , 1990 .