Next Article in Journal
Effects of Bacterioruberin-Rich Haloarchaeal Carotenoid Extract on the Thermal and Oxidative Stabilities of Fish Oil
Previous Article in Journal
The Discovery of Indole-2-carboxylic Acid Derivatives as Novel HIV-1 Integrase Strand Transfer Inhibitors
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Molecules
Volume 28
Issue 24
10.3390/molecules28248021
molecules-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Rosa rugosa Low Caloric Fiber Protein Preparations Rich in Antioxidant Flavanols and Ellagitannins

by
Joanna Milala
1,*,
Monika Kosmala
1,*,
Michał Sójka
1,
Krzysztof Kołodziejczyk
2,
Robert Klewicki
1,
Magdalena Król
1,
Elżbieta Karlińska
1 and
Edward Rój
3
1
Institute of Food Technology and Analysis, Lodz University of Technology, B. Stefanowskiego 2/22, 90-537 Łódź, Poland
2
Department of Sugar Industry and Food Safety Management, Lodz University of Technology, Wólczańska 171/173, 90-530 Łódź, Poland
3
Łukasiewicz Research Network—New Chemical Syntheses Institute, Tysiąclecia Państwa Polskiego 13a, 24-110 Puławy, Poland
*
Authors to whom correspondence should be addressed.
Molecules 2023, 28(24), 8021; https://doi.org/10.3390/molecules28248021
Submission received: 7 November 2023 / Revised: 6 December 2023 / Accepted: 7 December 2023 / Published: 9 December 2023
(This article belongs to the Section Food Chemistry)
Browse Figure
Versions Notes

Abstract

:
Defatted seed residues after the extraction of rose oil have their potential not fully described in the existing literature. The aim of this study was to determine and characterize the components important for the human body that are found in Rosa rugosa defatted seeds, including dietary fibers, proteins, selected minerals, polyphenols and antioxidant activity. Rosa rugosa seeds defatted with CO2 in supercritical conditions are a rich source of dietary fibers (approx. 65%) and proteins (15%); their macronutrients include the following: Ca (175.9), Mg (83.9), K (199.2) and Na (3.5 mg/100 g). They also contain polyphenols, including flavanols (0.9%) and total ellagic acid (0.5%), and they exhibit antioxidant activity (143.8 µM TAEC/g). Tellimagrandin I and II and rugosin A were found in the extracts, and ellagitannins with a yet-indeterminate structure were also present. The seeds also contained ellagitannin derivatives—galloyl-HHDP-glucose and bis-HHDP-glucose—at the same time, and they are characterized by a low-fat content—0.4%. The energy value of defatted rose seeds is about half the energy value of popular seeds used in the food industry. The findings of the present study suggest that defatted rosehip seeds, the by-product of rosehip processing, could be an important source of bioactive components like dietary fibers, flavanols, ellagitannins and mineral compounds. Therefore, defatted rose seeds are very promising and require further research, because they can potentially be used as a natural source of chemopreventive agents.

Graphical Abstract

1. Introduction

The rose (genus Rosa) includes about 120–200 species found mainly in the temperate zone of the northern hemisphere. In Europe, there are about 30 species, while 14–20 of them grow in Poland, in the wild. The probable cradle of roses is East Asia, in particular the area of China where the species varies the most. The geographical distribution of this plant varies greatly. The rose is found in natural habitats almost all over Europe, Asia Minor and North Africa. In Poland, it is often found in thickets, on the edges of forests, clearings, at the border of fields and along roads [1,2,3,4].
The wrinkled rose (Rosa rugosa) comes from East Asia. This species is widely cultivated, but it is also very commonly found in a feral form. The bush grows to a height of 2 m; it has thick erect stems with numerous runners. Shoots are gray, felt-hairy and densely covered with spines. The characteristic mossy pseudo-fruits of the rose are quite soft, flattened, up to 3 cm in diameter and weigh about 5 g and are orange red in color [4].
Rosa rugosa fruit and flakes are used in the food industry as an addition to jams, preserves, fruit purees, desserts for children and syrups. In the pharmaceutical industry, they are used for the production of vitamin preparations and herbal teas. Rosehip seeds have been evidenced to exhibit a series of biological activities such as gastrointestinal protection and diabetic, anti-aging and immunity-enhancing properties. They are the source of many ingredients, including, above all, phenolic components and mainly hydrolysable tannins [5,6,7] but also other nutrients such as fatty acids, terpenes, tocopherols, carotenoids, proteins, sugars and minerals [8,9]. Rose seeds are rich in unsaturated fatty acids (oleic acid and linoleic acid). Oils received from seeds of Rosa plants are common on the market and recommended for nutritional, cosmetic, and pharmaceutical purposes. Rosehip seeds may be offered as dietary supplements and as an additive in functional foods [10,11]. The cosmetics industry uses fruit extracts and seed oil for the production of cosmetic preparations [12], especially in preparations with anti-wrinkle properties, due to the elastase-inhibitor activity of rosehip seeds [11].
Polysaccharide-rich fractions (crude polysaccharides; CPL) from various R. rugosa achenes containing sugars, proteins and phenolic compounds have the ability to inhibit hyaluronidase activity. This can have an impact on the functioning of connective tissues, inflammatory processes, tumor invasion and metastasis [13].
R. rugose seeds can be recommended as an oil source in the skin care, cosmetic and dermatology industry thanks to their most desirable oil characteristics, in addition to being a source of the fatty acids required in terms of health [14]. In the literature, there are some data on the use of seeds after oil extraction from plants, such as camelina seeds and sophia seeds [15], grape seeds [16,17], poppy seeds [17], flaxseeds [18], blackcurrant and strawberry seeds [19], to obtain polyphenolic extracts or to fortify foods like cookies and breads. Available literature data indicate that defatted seeds of plants from the Rosacea family (waste after the oil extraction process) obtained from raspberries, strawberries or blackberries may be a source of many valuable nutrients and bioactive substances like dietary fibers and polyphenols [20,21,22]. These components have a beneficial pro-health effect. Polyphenols have been associated with a reduced risk of cardiovascular diseases and cancer. They have been attributed to several features, including antioxidant properties and free-radical scavenging activities [23,24]. Dietary fibers are essential for the proper functioning of the intestines, and they also lower the content of cholesterol and glucose in the blood [20,21].
Defatted seed residues after the extraction of rose oil have their potential not fully described in the existing literature. According to Moure et al. [25] and Concha et al. (2006) [26], Rosa rubignosa defatted residues are a source of dietary fibers, and these authors found that they can be a source of polyphenol preparations with high antioxidant activity. Rosa rubignosa defatted residues are a source of dietary fibers. They can be also a source of polyphenol preparations with a high antioxidant activity. So far, there are no studies on the content of bioactive ingredients such as flavanols and ellagitannins in defatted rose seeds as well as on the possibilities of the waste management of such products. That is why the aim of this study was to determine and characterize the components important for the human body, dietary fibers, proteins, selected minerals and polyphenols, in Rosa rugosa defatted seeds.

2. Results and Discussion

Defatted rose seeds were a rich source of fibers (65%) and proteins (15%); they contained moderate amounts of metabolizable carbohydrates (12%), minerals (such as ash 2.6%) and small amounts of fats (0.4%) (Table 1.). The energy value of the defatted seeds was 241 kcal/100 g on average. This value is much lower than the caloric value (energy value) of seeds used in the production of foodstuffs and/or consumed directly by humans, e.g., pumpkin seeds (446 kcal/100 g), sunflower seeds (584 kcal/100 g), sesame seeds (572 kcal/100 g) or linseeds (533 kcal/100 g) [27].
A statistical analysis showed significant differences in the composition of the tested samples obtained from different batches of the raw material. These differences may be the result of different origins of the starting material and different conditions of the de-oiling process in which individual batches of waste material were obtained. Comparing the obtained results on the composition of defatted seeds with the literature data from Kosmala et al. [20,21], it can be concluded that the dominant component, i.e., dietary fibers, is at a similar level compared to the content in defatted strawberry seeds (68.61%) and is slightly lower than that in defatted blackberry seeds (72.7%) or in defatted raspberry seeds (73.71%). Defatted rose seeds have a protein content similar to that of defatted strawberry seeds (15.62%), and it is higher than defatted blackberry seeds (10.5%) or defatted raspberry seeds (10.42%). In addition, rose seeds contain slightly more ash than defatted blackberry seeds (1.8%) or raspberries (1.81%) and, in two cases, is less than defatted strawberry seeds (3.63%).
The content of minerals showed a significant fluctuation in the samples from the individual batches. The mean content of calcium was 175.9 ± 62.1 mg/100 g, and that of magnesium was 83.9 ± 20.5 mg/100 g, that of potassium was 199.2 ± 92.2 mg/100 g and that of sodium was 3.5 ± 1.2 mg/100 g. The obtained results are consistent with the literature data. The potassium content of rose fruits, in the whole fruits and fruit parts, is very diverse. According to Kazaz at al. [28], potassium content in the damask rose was from 2243 mg/kg to 12,454 mg/kg and between 3231 mg/kg and 14,545 mg/kg in the dog rose. Demir and Özcan (2001) [29] reported a potassium level of 890.5–1023.9 mg/kg, and Ercisli [30] reported 5467 ppm and Kovacs et al. [31] 4200–11,900 ppm in various rose species. According to Kazaz at al. [28], calcium contents of the damask rose and canina rosehip fruits and fruit parts were found to be between 3885 (seeds)—11,162 (fruit flesh) mg/kg—and 3800 (seeds)—8442 mg/kg (fruit flesh). Demir and Özcan [29] reported that the Ca contents in rosehip fruits range between 133.3–146.7 ppm and Ercisli [30] reported them as 2867 ppm. The magnesium contents in the fruits and fruit parts of Rosa damascene and Rosa canina amounted to 441–2175 mg/kg, and the sodium contents ranged from 98 to 163 mg/kg [28].
Table 2 presents the antioxidant activity and content of the selected groups of polyphenols, as determined by the HPLC method, in defatted rose seeds.
The research data show that defatted rose seeds are sources of antioxidants, primarily of flavanols (801 ÷ 944 mg/100 g) and ellagic acid (326 ÷ 901 mg/100 g), bound or (in a smaller amount) free. The main representative of ellagitannins is ellagitannin calculated with a molecular weight of 1870 ((negative molecular ion peaks [M − H]− at m/z 934 z = 2) (139 ÷ 291 mg/100 g)). The antioxidant capacity, measured by the DDPPH method, is 120.3–183.0 µM TAEC/g.
Particular batches of defatted seeds differed significantly in the content of ellagic acid. However, the differences in the content of flavanols were statistically insignificant. The literature data confirm the presence of the above-mentioned groups of compounds in roses. The authors of [32] state that the content of ellagitannins in Rosa rugosa fruits is up to 110 mg per 100 g of fresh raw material. The second dominant group of polyphenolic compounds in the obtained extracts were procyanidins. Teleszko [33] indicates that the content of procyanidin polymers in Rosa rugosa fruits exceeds 25,600 μg/g DM, whereas Cunja et al. [34] and Milala et al. [1] show the presence of flavonols in pseudo-rose fruits at a level of 41.2–117 mg/100 g DM, depending on the variety. Research by Koczko et al. [7] shows that Rosa species, due to their antioxidant properties, should be considered potential ingredients of functional foods The relationship (correlation) between the antioxidant activity and the content of the determined substances was examined, and it showed a significant influence of the content of the total ellagic acid and main ellagitannins on the antioxidant potential (Table 3).
A complete list of the polyphenol compounds found in defatted Rosa rugosa seeds is given in Table 4.
In addition to the dominant ellagitannin (negative molecular ion peaks [M − H]− at m/z 934 z = 2), tellimagrandin I and II and rugosin A were also found in each of the extracts. In addition, ellagitannins with a yet-indeterminate structure were present. The extract also contained ellagitannin derivatives—galloyl-HHDP-glucose and bis-HHDP-glucose. Procyanidins were also found.
Flavonoids were present in the defatted seeds, and one of the most important glycosides was tiliroside. Free kaempferol and quercetin and glycoside derivatives of these compounds were also detected.
So far, the literature references pay little attention to Rosa rugosa seeds, including defatted ones. Much more attention was paid to the pseudo-fruits and flowers of plants belonging to the Rosa genus. Fecka [8] investigated the qualitative composition of Rosa canina pseudo-fruits; the presence of tellimagrandin I and II as well as monomeric and dimeric rugosines (A, B, D and E) were found. Wang et al. [39] and Olennikov et al. [40] report that among the tannins found in the Rosa genus, there are tellimagrandins I and II, rugosin A–E, roshenins A–E, agrimoinic acid, agrimoniin, sanguiin H-2, H-4, H-2, and H-6, casuarictin, stachuarin, lambertianin A and others. Ouerghemmi et al. [41] found that the extracts of rose leaves contain kaempferol 3-O-rutinoside, kaempferol 3-O-glucoside and keamferol 7-O-glucoside. The results of research conducted by the same author, Fecka [7], showed that rose seeds contain tiliroside and astragalin. As a result of research performed by Buchwald et al. [4], it was found that rosehips contain cyanidin-3-O-glucoside, cyanidin-3,5-diglucoside, peonidin-3-glucoside, quercetin, isoquercetin, astragalin, rutin, and also flavonoid glycosides. Mármol et al. [35] confirm that tiliroside is present in the acetone extracts of pseudo-fruits and rose seeds. Hvattumet et al. [43] confirm the presence of quercetin and its glycosides in rose fruits.

3. Materials and Methods

3.1. Material

The research material was defatted seeds of Rosa rugosa, obtained from Łukasiewicz-New Chemical Syntheses Institute in Puławy (Poland), after oil extraction by supercritical extraction with carbon dioxide. The supercritical fluid extraction of three batches of seeds was performed using an “ELAB” pilot plant, made at Łukasiewicz-INS, obtaining defatted seeds (SFE s. 1, SFE s. 2 and SFE s. 3). Before extraction, the seeds were grounded in a roll mill to facilitate the entrance of CO2 to the inner part of the seeds. Extraction was conducted under 30 MPa, at 50 °C, and the CO2 mass flow rate was 0.023 kg/s, and the extraction yield was 10–14%. The extraction time was 3.5 h, and the mass of the extraction material was 5 kg. The CO2 consumption amounted to 57.96 kg CO2/kg d.m. (dry mass).

3.2. Determination of the Nutritional Composition

Analyses of preparations: AOAC methods were used to determine the dry matter and ash, 940.26; proteins, 920.152; crude fats, 930.09; and total dietary fiber (TDF), 985.29 [45]. The metabolized carbohydrate content (MC) and the energy value (EV) were calculated using the formulas below [46]:
“MC” = “100%−”(P + F + A + DF + W)
“EV” = “MC”⋅4 + P⋅4 + F⋅9 + DF⋅2
where P = protein content [%]; F = fat content [%]; A = ash content [%]; DF = dietary fiber content [%]; W = water content [%].

3.3. Mineral Content

The contents of elements were determined as previously described by Sójka et al. [47]. The samples were calcined in a furnace at 550 °C for 16 h. The ash was then solubilized in 1 mol/L HNO3, and minerals were analyzed by the atomic absorption spectroscopy (AAS) method (SOLAAR 969 AAS spectrometer, Unicam, Ilminster, UK).

3.4. HPLC-PDA Measurement of Polyphenols

Polyphenol (free ellagic acid and main ellagitannin) content: The extraction of polyphenols was performed with the following solution: acetone:water:formic acid (70:29.9:0.1 v/v/v). A total of 500 mg of the material was mixed with 4 mL of a solvent and was sonified for 15 min. Next, the mixture was centrifuged at 14,000× g, and the solution was decanted. This procedure was repeated twice with 3 mL of solvents. Extracts were transferred to a 10 mL measuring flask and were filled up with solvents.
Total ellagic acid: A total of 100 mg of the material, 0.5 mL of 70% glycerol and 75 µL of concentrated TFA were poured into a 2 mL flask, then mixed and hydrolyzed for 18 h at 95 ± 1 °C. Then, the sample was quantitatively transferred into a 5 mL measuring flask and filled up with methanol [48].
The polyphenols and total ellagic acid were analyzed in the HPLC Smartline (Knauer, Berlin, Germany) chromatograph with a PDA detector. A Phenomenex Gemini 5u C18 110a (250 × 4.60 mm; 5 μm, Phenomenex, Torrance, CA, USA) column was kept at 35 °C, and the flow rate was 1.25 mL/min at an injection volume of 20 μL. Phase A was 0.05% (v/v) phosphoric acid in water and phase B was 83/20/17 (v/v/v) acetonitrile/methanol/water. The gradient was as follows: 0–5 min, 4% of phase B; 5–12.5 min, 4–15% of phase B; 12.5–42.5 min, 15–40% of phase B; 42.5–51.8 min, 40–50% of phase B; 51.8–53.4 min, 50–55% of phase B; and 53.4–55 min, 4% of phase B. Detection conditions were as follows: 360 nm for ellagic acid and 250 nm for ellagitannins. Ellagic acid and ellagitannin agrimoniin were used as standards. The method parameters are described in [44].

3.5. HPLC-FD Measurement of Flavanols

Proanthocyanidin degradation in an acidic environment with an overdose of phloroglucinol were performed according to Sójka et al. [48]: a total of 20 mg of the sample was mixed with 800 μL of a methanol solution containing phloroglucinol (75 g/L) and ascorbic acid (15 g/L). Phloroglucinolysis was started by adding 400 μL of 0.2 mol/L of hydrochloric acid in methanol and lasted for 30 min at 50 °C, and then the reaction was stopped by adding 600 μL of a 40 mmol/L sodium acetate solution and by being placed in an ice bath. The samples were centrifuged for 5 min at 12,000× g and were diluted with a 40 mmol/L sodium acetate solution. A chromatograph with a fluorescence detector (FD) RF-10AXL (Shimadzu, Tokyo, Japan) equipped with a Phenomenex Gemini 5u C18 110a (250 × 4.60 mm; 5 μm) column was used. The gradient was 0–10 min, 4−7% phase B; 10–27 min, 7–30% phase B; 27–29 min, 30–70% phase B; 29–34 min, 70% phase B; 34–35 min, 70–4% phase B; and 35–40 min, 4% phase B. Phase A consisted of a 2.5% water solution (v/v) of acetic acid, and phase B consisted of 80% (v/v) acetonitrile in water. The flow rate was 1 mL/min, and the temperature was 25 °C. The identification was conducted using the following standards: (−)-epicatechin, (+)-catechin, (−)-epicatechin-phloroglucinol and (+)-catechin-phloroglucinol. Quantitative analyses of the released flavonols, namely, (+)-catechin and (−)-epicatechin and phloroglucinol adducts, were conducted on the basis of chromatograms recorded with the FD set at a 278 nm excitation wavelength and a 360 nm emission wavelength. The method parameters are described in [49].

3.6. Qualitative Measurement of Selected Polyphenols by UHPLC-DAD-MS

Ultra-High-Performance Liquid Chromatography and Electrospray Ionization Mass Spectrometry (UHPLC-ESI-MS): A Dionex UltiMate 3000 UHPLC apparatus (Thermo Fisher Scientific, Waltham, MA, USA) coupled with a Thermo Scientific Q Exactive quadrupole ion trap mass spectrometer was used. A Phenomenex Luna 5 μm C18 column (250 × 4.6 mm) was used. Phase A was formic acid in water (1/99 v/v), and phase B was acetonitrile\methanol\water (63/20/17 v/v). The gradient was 0–6 min, 5% of phase B; 6–36 min, 5–28% of phase B; 36–48 min, 28–73% of phase B; 48–54 min, 73% of phase B; 54–60 min, 73–5% of phase B; and 60–70 min, 5% of phase B. The DAD detector recorded spectra simultaneously in the range of 200–600 nm, and the mass spectrometer recorded spectra in negative mode (H-ESI source). The source parameters were set as follows: vaporizer temperature, 500 °C; ion spray voltage, 4 kV; and capillary temperature, 400 °C; the sheath gas and auxiliary gas flow rates were 75 and 20 units, respectively. In full MS/dd-MS2 scanning mode, the mass range was set at m/z 200–2000 and the collision energy at 20 eV. Data were collected using the Xcalibur software 3.063 (Thermo Fisher Scientific, Waltham, MA, USA). The results of the polyphenol identification are given in Table 4.

3.7. Antioxidant Activity

Antioxidant activity was measured by the DPPH method and calculated as Trolox equivalent (TEAC) [50].

3.8. Statistics

All analyses were performed in duplicates. The test results were subjected to a statistical analysis using the one-way analysis of variance. For the obtained results, Duncan’s post-hoc test was performed at a significance level of α ≤ 0.05. The calculations were performed in the Statistica 10 software (Stat Soft, Tulsa, USA).

4. Conclusions

Rose seeds defatted with CO2 in supercritical conditions are a rich source of dietary fibers (approx. 65%) and proteins (15%). At the same time, they are characterized by a low-fat content—0.4%. Moreover, the seeds are a source of macronutrients, including Ca (175.9), Mg (83.9 mg/100 g), K (199.2 mg/100 g) and Na (3.5 mg/100 g). Defatted in supercritical conditions, rose seeds show antioxidant activity (143.8 µM TAEC/g) and contain polyphenols, including flavanols (0.9%) and total ellagic acid (0.5%). Tellimagrandin I and II, rugosin A and sanguiin H-6 with a gallic group were found in the extracts, and ellagitannins with a yet-indeterminate structure were present. The extract also contained ellagitannin derivatives—galloyl-HHDP-glucose and bis-HHDP-glucose. The energy value of defatted rose seeds is about half the energy value of popular seeds used in the food industry. The findings of the present study suggest that defatted rosehip seeds, the by-product of rosehip processing, could be an important source of bioactive components as dietary fibers, flavanols, ellagitannins and mineral compounds. Therefore, defatted rose seeds are very promising and require further research, because they can potentially be used as a natural source of chemopreventive agents.
There is a need for further research to determine the biological effect of defatted rose seeds as well as the possibility of obtaining valuable polyphenol extracts.

Author Contributions

Conceptualization, J.M.; methodology—J.M., M.K. (Monika Kosmala), M.S. and E.R.; software—J.M.; investigation, J.M. and E.K.; writing—original draft, J.M.; formal analysis, J.M., K.K. and M.K. (Magdalena Król); writing—review and editing, J.M., M.K. (Monika Kosmala) and R.K. All authors have read and agreed to the published version of the manuscript.

Funding

This work was financed from the statutory funds of the Institute of Food Technology and Analysis, the Faculty of Biotechnology and Food Sciences, Lodz University of Technology.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data presented in this study are available on request from the corresponding author. The data are not publicly available due to due to the volume of the partial data.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Milala, J.; Sójka, M.; Król, K.; Buczek, M. Charakterystyka składu chemicznego owoców Rosa pomifera ‘Karpatia’. Żywność Nauka Technol. Jakość 2013, 5, 154–167. [Google Scholar]
  2. Cendrowski, A.; Kalisz, S.; Mitek, M. Properties and applications of rose hips in food processing. Żywność Nauka Technol. Jakość 2012, 4, 24–31. [Google Scholar] [CrossRef]
  3. Fatrcová-Šramková, K.; Brindza, J.; Ivanišová, E.; Juríková, T.; Schwarzová, M.; Horčinová Sedláčková, V.; Grygorieva, O. Morphological and antiradical characteristics of Rugosa rose (Rosa rugosa Thunb.) fruits canned in different kind of honeys and in beverages prepared from honey. Potravin. Slovak J. Food Sci. 2019, 13, 497–506. [Google Scholar] [CrossRef] [PubMed]
  4. Buchwald, W.; Zieliński, J.; Mścisz, A.; Adamczak, A.; Mrozikiewicz, P.M. Aktualny stan i perspektywy badań róż owocowych. [Current research on roses and their perspectives]. Herba Pol. 2007, 53, 85–89. [Google Scholar]
  5. Fascella, G.; D’Angiolillo, F.; Mammano, M.M.; Amenta, M.; Romeo, F.V.; Rapisarda, P.; Ballistreri, G. Bioactive compounds and antioxidant activity of four rose hip species from spontaneous Sicilian flora. Food Chem. 2019, 289, 56–64. [Google Scholar] [CrossRef] [PubMed]
  6. Koczka, N.; Stefanovits-Bányai, É.; Ombódi, A. Total Polyphenol Content and Antioxidant Capacity of Rosehips of Some Rosa Species. Medicines 2018, 5, 84. [Google Scholar] [CrossRef] [PubMed]
  7. Fecka, I. Qualitative and quantitative determination of hydrolysable tannins and other polyphenols in herbal products from meadowsweet and dog rose. Phytochem. Anal. 2009, 20, 177–190. [Google Scholar] [CrossRef] [PubMed]
  8. Bhave, A.; Schulzova, V.; Chmelarova, H.; Mrnka, L.; Hajslova, J. Assessment of rosehips based on the content of their biologically active compounds. J. Food Drug Anal. 2017, 25, 681–690. [Google Scholar] [CrossRef]
  9. Mannozzi, C.; Foligni, R.; Scalise, A.; Mozzon, M. Characterization of lipid substances of rose hip seeds as a potential source of functional components: A review. Italian J. Food Sci. 2020, 32, 721–733. [Google Scholar] [CrossRef]
  10. Kulaitienė, J.; Medveckienė, B.; Levickienė, D.; Vaitkevičienė, N.; Makarevičienė, V.; Jarienė, E. Changes in Fatty Acids Content in Organic Rosehip (Rosa spp.) Seeds during Ripening. Plants 2020, 9, 1793. [Google Scholar] [CrossRef]
  11. Chae, S.-H.; Lee, Y.-S.; Kim, J.-H.; Han, T.-H.; Ku, K.-M. Metabolite and Elastase Activity Changes in Beach Rose (Rosa rugosa) Fruit and Seeds at Various Stages of Ripeness. Plants 2021, 10, 1283. [Google Scholar] [CrossRef] [PubMed]
  12. Turan, S.; Solak, R.; Kiralan, M.; Ramadan, M.F. Bioactive lipids, antiradical activity and stability of rosehip seed oil under thermal and photo-induced oxidation. Grasas Aceites 2018, 69, 248. [Google Scholar] [CrossRef]
  13. Olech, M.; Nowacka-Jechalke, N.; Masłyk, M.; Martyna, A.; Pietrzak, W.; Kubiński, K.; Załuski, D.; Nowak, R. Polysaccharide-Rich Fractions from Rosa rugosa Thunb.—Composition and Chemopreventive Potential. Molecules 2019, 24, 1354. [Google Scholar] [CrossRef] [PubMed]
  14. Kayahan, S.; Ozdemir, Y.; Gulbag, F. Functional Compounds and Antioxidant Activity of Rosa Species Grown in Turkey. Erwerbs-Obstbau 2023, 65, 1079–1086. [Google Scholar] [CrossRef]
  15. Rahman, M.J.; Costa de Camargo, A.; Shahidi, F. Phenolic profiles and antioxidant activity of defatted camelina and Sophia seeds. Food Chem. 2018, 240, 917–925. [Google Scholar] [CrossRef] [PubMed]
  16. Duba, K.S.; Casazza, A.A.; Mohamed, H.B.; Perego, P.; Fiori, L. Extraction of polyphenols from grape skins and defatted grape seeds using subcritical water: Experiments and modeling. Food Bioprod. Process. 2015, 94, 29–38. [Google Scholar] [CrossRef]
  17. Aksoylu, Z.; Çağindi, Ö.; Köse, E. Effects of blueberry, grape seed powder and poppyseed incorporation on physicochemical and sensory properties of biscuit. J. Food Qual. 2015, 38, 164–174. [Google Scholar] [CrossRef]
  18. Gutiérrez, C.; Rubilar, M.; Jara, C.; Verdugo, M.; Sineiro, J.; Shene, C. Flaxseed and flaxseed cake as a source of compounds for food industry. J. Soil Sci. Plant Nutr. 2010, 10, 454–463. [Google Scholar] [CrossRef]
  19. Korus, J.; Juszczak, L.; Ziobro, R.; Witczak, M.; Grzelak, K.; Sójka, M. Defatted strawberry and blackcurrant seeds as functional ingredients of gluten-free bread. J. Texture Stud. 2012, 43, 29–39. [Google Scholar] [CrossRef]
  20. Kosmala, M.; Zduńczyk, Z.; Juśkiewicz, J.; Jurgoński, A.; Karlińska, E.; Macierzyński, J.; Jańczak, R.; Rój, E. Chemical composition of defatted strawberry and raspberry seeds and the effect of these dietary ingredients on polyphenol metabolites, intestinal function, and selected serum parameters in rats. J. Agric. Food Chem. 2015, 63, 2989–2996. [Google Scholar] [CrossRef]
  21. Kosmala, M.; Jurgoński, A.; Juśkiewicz, J.; Karlinśka, E.; Macierzyński, J.; Rój, E.; Zduńczyk, Z. Chemical Composition of Blackberry Press Cake, Polyphenolic Extract, and Defatted Seeds, and Their Effects on Cecal Fermentation, Bacterial Metabolites, and Blood Lipid Profile in Rats. J. Agric. Food Chem. 2017, 65, 5470–5479. [Google Scholar] [CrossRef] [PubMed]
  22. Grzelak-Błaszczyk, K.; Karlińska, E.; Grzęda, K.; Rój, E.; Kołodziejczyk, K. Defatted strawberry seeds as a source of phenolics, dietary fiber and minerals. LWT 2017, 84, 18–22. [Google Scholar] [CrossRef]
  23. Mendonça, R.D.; Carvalhod, N.C.; Martin-Moreno, J.M.; Pimenta, A.M.; Lopes, A.C.S.; Gea, A.; Martinez-Gonzalez, M.A.; Bes-Rastrollo, M. Total polyphenol intake, polyphenol subtypes and incidence of cardiovascular disease: The SUN cohort study. Nutr. Metab. Cardiovasc. Dis. 2019, 29, 69–78. [Google Scholar] [CrossRef]
  24. Yi, J.; Li, S.; Wang, C.; Cao, N.; Qu, H.; Cheng, C.; Wang, Z.; Wang, L.; Zhou, L. Potential applications of polyphenols on main ncRNAs regulations as novel therapeutic strategy for cancer. Biomed. Pharmacother. 2019, 113, 108703. [Google Scholar] [CrossRef] [PubMed]
  25. Moure, A.; Franco, D.; Santamaría, R.I.; Soto, C.; Sineiro, J.; Domínguez, H.; Zúñga, M.E.; Núñez, M.J.; Chamy, R.; López-Munguía, A.; et al. Enzyme-aided alternative processes for the extraction of oil from Rosa rubiginosa. JAOC 2001, 78, 437–439. [Google Scholar] [CrossRef]
  26. Concha, J.; Soto, C.; Chamy, R.; Zúñiga, M.E. Effect of Rosehip Extraction Process on Oil and Defatted Meal Physicochemical Properties. JAOCS 2006, 83, 771–775. [Google Scholar] [CrossRef]
  27. FoodData Central. Available online: https://fdc.nal.usda.gov (accessed on 1 October 2022).
  28. Kazaz, S.; Baydar, H.; Erbas, S. Variations in Chemical Compositions of Rosa damascena Mill. and Rosa canina L. Fruits. Czech J. Food Sci. 2009, 27, 178–184. [Google Scholar] [CrossRef]
  29. Demir, F.; Özcan, M. Chemical and technological properties of rose (Rosa canina L.) fruits grown wild in Turkey. J. Food Eng. 2001, 47, 333–336. [Google Scholar] [CrossRef]
  30. Ercisli, S. Chemical composition of fruits in some rose (Rosa spp.) species. Food Chem. 2007, 104, 1379–1384. [Google Scholar] [CrossRef]
  31. Kovacs, S.; Facsar, G.; Laszlo, U.; Toth, M. Phenological, morphological characteristics of some rose species found in Hungary. Acta Hortic. 2004, 690, 71–76. [Google Scholar] [CrossRef]
  32. Koponen, J.M.; Happonen, A.M.; Mattila, P.H.; Torronen, A.R. Contents of anthocyanins and ellagitannins in selected foods consumed in Finland. J. Agric. Food Chem. 2007, 55, 1612–1619. [Google Scholar] [CrossRef] [PubMed]
  33. Cendrowski, A.; Ścibisz, I.; Mitek, M.; Kieliszek, M.; Kolniak-Ostek, J. Profile of the Phenolic Compounds of Rosa rugosa Petals. J. Food Qual. 2017, 2017, 7941347. [Google Scholar] [CrossRef]
  34. Cunja, V.; Mikulic-Petkovsek, M.; Zupan, A.; Stampar, F.; Schmitzer, V. Frost decreases content of sugars, ascorbic acid and some quercetin glycosides but stimulates selected carotenes in Rosa canina hips. J. Plant Physiol. 2015, 178, 55–63. [Google Scholar] [CrossRef] [PubMed]
  35. Mármol, I.; Sánchez-de-Diego, C.; Jiménez-Moreno, N.; Ancín-Azpilicueta, C.; Rodríguez-Yoldi, M.J. Therapeutic Applications of Rose Hips from Different Rosa Species. Int. J. Mol. Sci. 2017, 18, 1137. [Google Scholar] [CrossRef] [PubMed]
  36. Salminen, J.P.; Karonen, M.; Lempa, K.; Liimatainen, J.; Sinkkonen, J.; Lukkarinen, M.; Pihlaja, K. Characterisation of proanthocyanidin aglycones and glycosides from rose hips by high-performance liquid chromatography–mass spectrometry, and their rapid quantification together with Vitamin C. J. Chromatogr. A 2005, 1077, 170–177. [Google Scholar] [CrossRef] [PubMed]
  37. Gu, D.; Yang, Y.; Bakri, M.; Chen, Q.; Xin, X.; Aisa, H.A. A LC/QTOF-MS/MS application to investigate chemical compositions in a fraction with protein tyrosine phosphatase 1B inhibitory activity from Rosa rugosa flowers. Phytochem. Anal. 2013, 24, 661–670. [Google Scholar] [CrossRef] [PubMed]
  38. Fetni, S.; Bertella, N.; Ouahab, A.; Zapater, J.M.M.; De Pascual, S.; Fernandez, T. Composition and biological activity of the Algerian plant Rosa canina L. by HPLC-UV-MS. Arab. J. Chem. 2017, 13, 1105–1119. [Google Scholar] [CrossRef]
  39. Wang, Y.; Zhao, Y.; Liu, X.; Li, J.; Zhang, J.; Liu, D. Chemical constituents and pharmacological activities of medicinal plants from Rosa genus. Chin. Herb. Med. 2022, 14, 187–209. [Google Scholar] [CrossRef]
  40. Cunja, V.; Mikulic-Petkovsek, M.; Stampar, F.; Schmitzer, V. Compound Identification of Selected Rose Species and Cultivars: An Insight to Petal and Leaf Phenolic Profiles. J. Am. Soc. Hortic. Sci. 2014, 139, 157–166. [Google Scholar] [CrossRef]
  41. Olennikov, D.N.; Chemposov, V.V.; Chirikova, N.K. Metabolites of Prickly Rose: Chemodiversity and Digestive-Enzyme-Inhibiting Potential of Rosa acicularis and the Main Ellagitannin Rugosin D. Plants 2021, 10, 2525. [Google Scholar] [CrossRef]
  42. Ouerghemmi, S.; Sebei, H.; Siracusa, L.; Ruberto, G.; Saija, A.; Cimino, F.; Cristani, M. Comparative study of phenolic composition and antioxidant activity of leaf extracts from three wild Rosa species grown in different tunisia regions: Rosa canina L.; Rosa moschata Herrm. and Rosa sempervirens L. Ind. Crops Prod. 2016, 94, 167–177. [Google Scholar] [CrossRef]
  43. Hvattum, E. Determination of phenolic compounds in rose hip (Rosa canina) using liquid chromatography coupled to electrospray ionisation tandem mass spectrometry and diode-array detection. Rapid Commun. Mass Spectrom. 2002, 16, 655–662. [Google Scholar] [CrossRef]
  44. Karlińska, E.; Romanowska, B.; Kosmala, M. The Aerial Parts of Agrimonia procera Wallr. and Agrimonia eupatoria L. as a Source of Polyphenols, and Especially Agrimoniin and Flavonoids. Molecules 2021, 26, 7706. [Google Scholar] [CrossRef] [PubMed]
  45. Horwitz, W.; Latimer, G.W. Official Methods of Analysis of AOAC International, 18th ed.; AOAC International: Rockville, MD, USA, 2007. [Google Scholar]
  46. de Menezes, E.W.; Grande, F.; Giuntini, E.B.; Lopes, T.D.V.C.; Dan, M.C.T.; Prado, S.B.R.; Melo Franco, B.D.G.; Charrondière, U.R.; Lajolo, F.M. Impact of dietary fiber energy on the calculation of food total energy value in the Brazilian Food Composition Database. Food Chem. 2016, 193, 128–133. [Google Scholar] [CrossRef] [PubMed]
  47. Sójka, M.; Kołodziejczyk, K.; Milala, J. Polyphenolic and basic chemical composition of black chokeberry industrial by-products. Ind. Crop. Prod. 2013, 51, 77–86. [Google Scholar] [CrossRef]
  48. Sójka, M.; Klimczak, E.; Macierzyński, J.; Kołodziejczyk, K. Nutrient and polyphenolic composition of industrial strawberry press cake. Eur. Food Res. Technol. 2013, 237, 995–1007. [Google Scholar] [CrossRef]
  49. Milala, J.; Piekarska-Radzik, L.; Sójka, M.; Klewicki, R.; Matysiak, B.; Klewicka, E. Rosa spp. Extracts as a Factor That Limits the Growth of Staphylococcus spp. Bacteria, a Food Contaminant. Molecules 2021, 26, 4590. [Google Scholar] [CrossRef]
  50. Kim, D.O.; Lee, K.W.; Lee, H.J.; Lee, C.Y. Vitamin C equivalent antioxidant capacity (VCEAC) of phenolic phytochemicals. J. Agric. Food Chem. 2002, 50, 3713–3717. [Google Scholar] [CrossRef]
Table 1. Chemical composition of seeds defatted with CO2 under supercritical conditions.
Table 1. Chemical composition of seeds defatted with CO2 under supercritical conditions.
Defatted SeedsSFE s.1SFE s.2SFE s.3Mean
Dry matter95.6 ± 0.0 b95.6 ± 0.1 b93.3 ± 0.1 a94.8 ± 1.3
Ash %2.4 ± 0.1 b3.5 ± 0.1 c1.9 ± 0.0 a2.6 ± 0.6
Ca mg/100 g152.0 ± 5.7 b246.4 ± 4.8 c129.3.0 ± 4.6 a175.9 ±62.1
Mg mg/100 g69.6 ± 2.6 a107.4 ± 1.7 b74.8 ± 0.9 a83.9 ± 20.5
K mg/100 g125.2 ±10.8 a302.5 ± 7.1 c170.0 ± 0.8 b199.2 ± 92.2
Na mg/100 g3.0 ± 0.4 a4.9 ± 0.2 b2.6 ± 0.1 a3.5 ± 1.2
Protein %15.1 ± 0.3 a15.0 ± 0.4 a14.1 ± 0.1 b14.7 ± 0.5
Dietary Fibers %66.1 ± 0.3 b61.2 ± 0.4 a67.4 ± 0.1 c64.9 ± 2.7
Metabolized carbohydrates, %11.3 ± 0.2 b15.6 ± 0.2 c9.7 ± 0.1 a12.2 ± 2.5
Fat %0.6 ± 0.1 b0.3 ± 0.1 a0.1 ± 0.0 a0.4 ± 0.2
Energy value, kcal/100 g243.5 ± 0.2 b247.8 ± 0.6 c231.1 ± 0.4 a240.8 ± 7.1
The same letters in the line are not statistically significant differences with p < 0.05.
Table 2. The antioxidant activity and content of selected groups of polyphenols in defatted rose seeds.
Table 2. The antioxidant activity and content of selected groups of polyphenols in defatted rose seeds.
PolyphenolsSFE s.1SFE s.2SFE s.3Mean
Main ellagitannin
mg/100 g		146.5 ± 7.3 a270.5 ± 11.3 b138.5 ± 0.7 a185.2 ± 74.0
Free ellagic acid
mg/100 g		12.1 ± 1.7 a33.1 ± 0.0 b11.7 ± 0.4 a19.0 ± 12.2
Total ellagic acid
mg/100 g		452.9 ± 20.9 b900.7 ± 59.6 c325.7 ± 22.9 a559.8 ± 302.0
Flavanols
mg/100 g		801.2 ± 12.4 a943.8 ± 83.4 a851.9 ± 12.2 a865.6 ± 72.3
Antioxidant activity
DPPH µM TAEC/g		128.0 ± 6.3 a183.0 ± 10 b120.3 ± 2.0 a143.8 ± 34.2
The same letters in the line are not statistically significant differences with p < 0.05.
Table 3. The relationship (correlation) between the antioxidant activity and the content of the determined substances.
Table 3. The relationship (correlation) between the antioxidant activity and the content of the determined substances.
VariableThe Spearman Rank-Order Correlation Coefficient Significant
Differences p < 0.0500
Total Ellagic AcidFree Ellagic AcidMain EllagitaninFlavanols
Antioxidant activity DPPH0.8857140.7714290.9428570.371429
Table 4. Qualitative composition of polyphenolic compounds in defatted Rosa rugosa seeds’ identification [7,35,36,37,38,39,40,41,42,43,44].
Table 4. Qualitative composition of polyphenolic compounds in defatted Rosa rugosa seeds’ identification [7,35,36,37,38,39,40,41,42,43,44].
RT
[min]		MS Data [m/z]MS/MS DataMW [g/mol]Compound
116.5[783.07]−783, 451, 301784Bis-HHDP-glucose
[633.07]−633, 301634HHDP-galloyl-glucose
218.2[783.07]−783, 451, 301784Bis-HHDP-glucose
[633.07]−633, 301634HHDP-galloyl-glucose
320.7[577.14]−425, 408, 407, 289, 137, 125578Procyanidin dimer
[785.09]−483, 419, 313, 301786di-O-galloyl-HHDP-glucose Tellimagrandin
421.65[865.2]−695, 577, 407, 287, 125866Procyanidin trimer
522.6[289.07]−245, 241, 125290Catechin
624.5[1153.26]−983, 865, 695, 577, 449, 287, 1251154Procyanidin tetramer
726.1[785.09]−633, 483, 419, 301786di-O-galloyl-HHDP-glucose Tellimagrandin I
928.56[635.09]−465, 313, 295, 223, 211, 193, 169, 125636Tri-O-galloyl-glucoside
1029.1[1153.26]−983, 865, 695, 577, 449, 287, 1251154Procyanidin tetramer
1129.4[933.07]−631, 451, 301934Ellagitannin
[865.2]−695, 577, 543, 451, 425, 407, 287,125866Procyanidin trimer
1230.55[935.08]−898, 765, 633, 463, 301936Galloyl bis HHDP- glucose
1332.8[1018.0]2−1691, 1567, 1265, 1209, 1059, 935, 897, 783, 633, 3012038Ellagitannin
1433.8[937.1]−785, 767, 741, 635, 465, 419, 301938Tri-galloyl-HHDP-glucose
Tellimagrandin II
1534.01[1105]−1061, 937, 917, 909, 891, 805, 785, 767, 749, 633, 615, 597, 465, 425, 301, 275, 169, 1251106Rugosin A
1635.39[787.1]−
[935]2−		635, 617, 483, 465, 447, 313, 295
1569, 1085, 1059, 935, 917, 787, 767, 633, 451, 301		788
1872		Tetragalloyl glucose
Ellagitannin
1736.12[934]2−1567, 1265, 1085, 935, 897, 783, 633, 3011870Ellagitannin
1837.08[615.1]−463, 301616Quercetin-galloylhexoside
[433.04]−301434Ellagic acid pentoside
1938.02[1085.08]−783, 633, 613, 451, 3011086Galloyl-castalagin
2038.4[301.0]− 302Ellagic acid
2139.02[463.09]−301464Quercetin hexoside
2239.73[939.11]− 769, 617, 599, 465, 447, 431, 169940Pentagalloylglucose
2339.99[477.1]−477, 313, 265, 169478not identified
2440.04[1085.08]−783, 633, 613, 451, 3011086Galloyl-castalagin
2541.53[433.08]−433, 301, 300434Ellagic acid pentoside
2642.45[447.09]−301448Quercetin 3-rhamnoside
2746.13[593.13]−463, 285594Tiliroside *
2846.3[301.04]− 302Quercetin
2948.6[285.04]− 286Kaempferol
* kaempferol-3-O-β-d-(6″-E-p-coumaroyl)-glucopyranoside.
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Milala, J.; Kosmala, M.; Sójka, M.; Kołodziejczyk, K.; Klewicki, R.; Król, M.; Karlińska, E.; Rój, E. Rosa rugosa Low Caloric Fiber Protein Preparations Rich in Antioxidant Flavanols and Ellagitannins. Molecules 2023, 28, 8021. https://doi.org/10.3390/molecules28248021

AMA Style

Milala J, Kosmala M, Sójka M, Kołodziejczyk K, Klewicki R, Król M, Karlińska E, Rój E. Rosa rugosa Low Caloric Fiber Protein Preparations Rich in Antioxidant Flavanols and Ellagitannins. Molecules. 2023; 28(24):8021. https://doi.org/10.3390/molecules28248021

Chicago/Turabian Style

Milala, Joanna, Monika Kosmala, Michał Sójka, Krzysztof Kołodziejczyk, Robert Klewicki, Magdalena Król, Elżbieta Karlińska, and Edward Rój. 2023. "Rosa rugosa Low Caloric Fiber Protein Preparations Rich in Antioxidant Flavanols and Ellagitannins" Molecules 28, no. 24: 8021. https://doi.org/10.3390/molecules28248021

APA Style

Milala, J., Kosmala, M., Sójka, M., Kołodziejczyk, K., Klewicki, R., Król, M., Karlińska, E., & Rój, E. (2023). Rosa rugosa Low Caloric Fiber Protein Preparations Rich in Antioxidant Flavanols and Ellagitannins. Molecules, 28(24), 8021. https://doi.org/10.3390/molecules28248021

Article Metrics

Back to TopTop