Search for Author, Title, Keyword
ORIGINAL ARTICLE
Strawberry Polyphenol-Rich Fractions Can Mitigate Disorders in Gastrointestinal Tract and Liver Functions Caused by a High-Fructose Diet in Experimental Rats
 
More details
Hide details
1
Department of Microbiology and Food Technology, Faculty of Agriculture and Biotechnology, Bydgoszcz University of Science and Technology, Kaliskiego 7, 85–796 Bydgoszcz, Poland
 
2
Department of Biological Functions of Food, Institute of Animal Reproduction and Food Research of the Polish Academy of Sciences, Tuwima 10, 10–748 Olsztyn, Poland
 
3
Institute of Food Technology and Analysis, Łódź University of Technology, Stefanowskiego 4/10, 90–924 Łódź, Poland
 
4
Department of Animal Nutrition, Lithuanian University of Health, Kaunas, Tilzes 18, LT-47181 Kaunas, Lithuania
 
5
Policlinico Veterinario Roma Sud, Ophthalmology, 00173 Rome, Italy
 
 
Submission date: 2021-07-21
 
 
Final revision date: 2021-10-11
 
 
Acceptance date: 2021-10-13
 
 
Online publication date: 2021-11-16
 
 
Publication date: 2021-11-16
 
 
Corresponding author
Ewa Żary-Sikorska   

Department of Microbiology and Food Technology, Faculty of Agriculture and Biotechnology, Bydgoszcz University of Science and Technology, Kaliskiego 7, 85–796 Bydgoszcz, Poland
 
 
Pol. J. Food Nutr. Sci. 2021;71(4):423-440
 
KEYWORDS
TOPICS
ABSTRACT
In the current study, it was hypothesized that the addition of strawberry polyphenol-rich fractions to a high-fructose diet mitigates disorders in liver functions, lipid metabolism, and in the antioxidant and pro-inflammatory status of rats. Therefore, a fraction rich in ellagitannins and proanthocyanidins (EP), and a fraction containing compounds of both mentioned classes of polyphenols and additionally anthocyanins (EPA), in doses of 0.28 and 0.70 g/100 g, respectively, were added to a standard or a high-fructose diet administered to rats for six weeks. The EPA fraction was more beneficial in alleviating the consequences of consuming excess fructose in the diet than the EP fraction. Probably, that fraction containing considerable amounts of carbohydrates was more extensively metabolized by intestinal bacteria, which resulted in higher levels of cecal short chain fatty acids (SCFAs) as well as cecal and urinal ellagitannin metabolites. As a further consequence, diet supplementation with the EPA fraction caused more favorable changes in the levels of serum interleukin 6 and serum antioxidant capacity of water-soluble substances (ACW), in atherogenicity index lg((triglyceride/high-density lipoprotein cholesterol), hepatic oxidized glutathione as well as reduced to oxidized glutathione ratio). Efforts should be made to develop strawberry polyphenol-rich preparations containing the preferred anthocyanins, which is, however, difficult due to the instability of this class of phenolic compounds during the technological process.
FUNDING
This research was supported by statutory funds from the Department of Biological Function of Food, Institute of Animal Reproduction and Food Research, Polish Academy of Sciences, Olsztyn, Poland; and Department of Microbiology and Food Technology, Faculty of Agriculture and Biotechnology, University of Science and Technology, Bydgoszcz, Poland.
REFERENCES (56)
1.
Aboonabi, A., Aboonabi, A. (2020). Anthocyanins reduce inflammation and improve glucose and lipid metabolism associated with inhibiting nuclear factor-kappaB activation and increasing PPAR-γ gene expression in metabolic syndrome subjects. Free Radical Biology and Medicine, 150, 30-39. https://doi.org/10.1016/j.free....
 
2.
AOAC, Official Methods of Analysis, 21st Edition - AOAC International. 2019. Available online: [https://www.aoac.org/official-...] (accessed 23 June 2020).
 
3.
Aura, A.M., Martin-Lopez, P., O'Leary, K.A., Williamson, G., Oksman-Caldentey, K.-M., Poutanen, K., Santos-Buelga, C. (2005). In vitro metabolism of anthocyanins by human gut microflora. European Journal of Nutrition, 44(3), 133-142. https://doi.org/10.1007/s00394....
 
4.
Awolade, P., Cele, N., Kerru, N., Gummidi, L., Oluwakemi, E., Singh, P. (2020). Therapeutic significance of β-glucuronidase activity and its inhibitors: A review. European Journal of Medicinal Chemistry, 187, art. no. 111921. https://doi.org/10.1016/j.ejme....
 
5.
Bauza-Kaszewska, J., Żary-Sikorska, E., Gugolek, A., Ligocka, A., Kosmala, M., Karlińska, E., Fotschki, B., Juśkiewicz, J. (2021). Synergistic antimicrobial effect of raspberry (Rubus idaeus L., Rosaceae) preparations and probiotic bacteria on enteric pathogens. Polish Journal of Food and Nutrition Sciences, 71(1), 51-59. https://doi.org/10.31883/pjfns....
 
6.
Bialonska, D., Ramnani, P., Kasimsetty, S.G., Muntha, K.R., Gibson, G.R., Ferreira, D. (2010). The influence of pomegranate by-product and punicalagins on selected groups of human intestinal microbiota. International Journal of Food Microbiology, 140(2-3), 175-182. https://doi.org/10.1016/j.ijfo....
 
7.
Botsoglou, N.A., Fletouris, D.J., Papageorgiou, G.E., Vassilopoulos, V.N., Mantis, A.J., Trakatellis, A.G. (1994). Rapid, sensitive, and specific thiobarbituric acid method for measuring lipid peroxidation in animal tissue, food and feedstuff samples. Journal of Agricultural and Food Chemistry, 42(9), 1931–1937. https://doi.org/10.1021/jf0004....
 
8.
Buzzini, P., Arapitsas, P., Goretti, M., Branda, E., Turchetti, B., Pinelli, P., Ieri, F., Romani, A. (2008). Antimicrobial and antiviral activity of hydrolysable tannins. Mini-Reviews in Medicinal Chemistry, 8(12), 1179–1187. https://doi.org/10.2174/138955....
 
9.
Cheng, S., Han, F., Wang, Y., Xu, Y., Qu, T., Ju, Y., Lu, Z. (2017). The red distribution width and the platelet distribution width as prognostic predictors in gastric cancer. BMC Gastroenterology, 17(1), art.no. 163. https://doi.org/10.1186/s12876....
 
10.
DeBosch, B.J., Chen, Z., Finck, B.N., Chi, M., Moley, K.H. (2013). Glucose transporter-8 (GLUT8) mediates glucose intolerance and dyslipidemia in high-fructose diet-fed male mice. Molecular Endocrinology, 27(11), 1887–1896. https://doi.org/10.1210/me.201....
 
11.
Elkhadragy, M.F., Abdel Moneim, A.E. (2017). Protective effect of Fragaria ananassa methanolic extract on cadmium chloride (CdCl2)-induced hepatotoxicity in rats. Toxicology Mechanisms and Methods, 27(5), 335–345. https://doi.org/10.1080/153765....
 
12.
EU Directive (2010/63/EU). Directive 2010/63/EU of the European Parliament and of the Council of 22 September 2010 on the protection of animals used for scientific purposes.
 
13.
Ertan, K., Türkyılmaz, M., Özkan, M. (2020). Color and stability of anthocyanins in strawberry nectars containing various co-pigment sources and sweeteners. Food Chemistry, 310, art. no. 125856. https://doi.org/10.1016/j.food....
 
14.
Folch, J., Lees, M., Sloane Stanley, G.H. (1957). A simple method for the isolation and purification of total lipids from animal tissues. Journal of Biological Chemistry, 226(1), 497-509. https://doi.org/10.1016/S0021-....
 
15.
Forbes-Hernández, T.Y., Gasparrin, M., Afrin, S., Cianciosi, D., González-Paramás, A.M., Santos-Buelga, C., Mezzetti, B., Quiles, J.L., Battino, M., Giampieri, F., Bompadre, S. (2017). Strawberry (cv. Romina) methanolic extract and anthocyanin-enriched fraction improve lipid profile and antioxidant status in HepG2 cells. International Journal of Molecular Sciences, 18(6), art. no. 1149. https://doi.org/10.3390/ijms18....
 
16.
Fotschki, B., Milala, J., Jurgoński, A., Karlińska, E., Zduńczyk, Z., Juśkiewicz, J. (2014). Strawberry ellagitannins thwarted the positive effects of dietary fructooligosaccharides in rat cecum. Journal of Agricultural and Food Chemistry, 62(25), 5871–5880. https://doi.org/10.1021/jf4056....
 
17.
Fotschki, B., Juśkiewicz, J., Jurgoński, A., Kołodziejczyk, K., Milala, J., Kosmala, M., Zduńczyk, Z. (2016). Anthocyanins in strawberry polyphenolic extract enhance the beneficial effects of diets with fructooligosaccharides in the rat cecal environment. PLOS ONE, 11(2), art. no. e0149081. https://doi.org/10.1371/journa....
 
18.
Fotschki, B., Juśkiewicz, J., Kołodziejczyk, K., Jurgoński, A., Kosmala, M., Milala, J., Ognik, K., Zduńczyk, Z. (2018). Protective effects of ellagitannin-rich strawberry extracts on biochemical and metabolic disturbances in rats fed a diet high in fructose. Nutrients, 10(4), art. no. 445. https://doi.org/10.3390/nu1004....
 
19.
Fuke, N., Nagata, N., Suganuma, H., Ota, T. (2019). Regulation of gut microbiota and metabolic endotoxemia with dietary factors. Nutrients, 11(10), art. no. 2277. https://doi.org/10.3390/nu1110....
 
20.
Giampieri, F., Tulipani, S., Alvarez-Suarez, J.M., Quiles, J.L., Mezzetti, B., Battino, M. (2012). The strawberry: Composition, nutritional quality, and impact on human health. Nutrition, 28(1), 9-19. https://doi.org/10.1016/j.nut.....
 
21.
Gonzalez-Barrio, R., Truchado P., Ito, H., Espín, J.C., Tomas-Barberan, F. (2011). UV and MS identification of urolithins and nasutins, the bioavailable metabolites of ellagitannins and ellagic acid in different mammals. Journal of Agricultural and Food Chemistry, 59(4), 1152–1162. https://doi.org/10.1021/jf1038....
 
22.
Hambly, R.J., Rumney, C.J., Cunningham, M., Fletcher, J.M.E., Rijken, P., Rowland, I.R. (1997). Influence of diets containing high and low risk factors for colon cancer on early stages of carcinogenesis in human-flora-associated (HFA) rats. Carcinogenesis, 18(8), 1535–1539. https://doi.org/10.1093/carcin....
 
23.
Hassimotto, N., Moreira, V., Nascimento, N., Souto, P., Teixeira, C., Lajolo, F.M. (2013). Inhibition of carrageenan-induced acute inflammation in mice by oral administration of anthocyanin mixture from wild mulberry and cyanidin-3-glucoside. BioMed Research International, 2013, art. no. 146716. https://doi.org/10.1155/2013/1....
 
24.
Hidalgo, M., Oruna-Concha, M.J., Kolida, S., Walton, G.E., Kallithraka, S., Spencer, J.P.E., Gibson, G.R., de Pascual-Teresa, S. (2012). Metabolism of anthocyanins by human gut microflora and their influence on gut bacterial growth. Journal of Agricultural and Food Chemistry, 60(15), 3882–3890. https://doi.org/10.1021/jf3002....
 
25.
Hillilä, M., Färkkilä, M.A., Sipponen, T., Rajala, J., Koskenpato, J. (2016). Does oral galactosidase relieve irritable bowel symptoms?. Scandinavian Journal of Gastroenterology, 51(1), 16–21. https://doi.org/10.3109/003655....
 
26.
Horne, R.G., Yu, Y., Zhang, R., Abdalqadir, N., Rossi, L., Surette, M., Sherman, P.M., Adeli, K. (2020). High fat-high fructose diet-induced changes in the gut microbiota associated with dyslipidemia in Syrian hamsters. Nutrients, 12(11), art. no. 3557. https://doi.org/10.3390/nu1211....
 
27.
Jarosławska, J., Juśkiewicz, J., Wróblewska, M., Jurgoński, A., Król, B., Zduńczyk, Z. (2011). Polyphenol-rich strawberry pomace reduces serum and liver lipids and alters gastrointestinal metabolite formation in fructose-fed rats. Journal of Nutrition, 141(10), 1777-1783. https://doi.org/10.3945/jn.111....
 
28.
Jurgoński, A., Juśkiewicz, J., Zduńczyk, Z. (2013). An anthocyanin-rich extract from Kamchatka honeysuckle increases enzymatic activity within the gut and ameliorates abnormal lipid and glucose metabolism in rats. Nutrition, 29(6), 898–902. https://doi.org/10.1016/j.nut.....
 
29.
Kang, I., Kim, Y.E., Tomás-Barberán, F.A., Espín, J.C., Chung, S. (2016). Urolithin A, C, and D, but not iso-urolithin A and urolithin B, attenuate triglyceride accumulation in human cultures of adipocytes and hepatocytes. Molecular Nutrition and Food Research, 60(5), 1129-1138. https://doi.org/10.1002/mnfr.2....
 
30.
Kennedy, J.A., Jones, G.P. (2001). Analysis of proanthocyanidin cleavage products following acid-catalysis in the presence of excess phloroglucinol. Journal of Agricultural and Food Chemistry, 49(4), 1740-1746. https://doi.org/10.1021/jf0010....
 
31.
Kosmala, M., Zduńczyk, Z., Juśkiewicz, J., Jurgoński, A., Karlińska, E., Macierzyński, J., Jańczak, R., Rój, E. (2015). 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. Journal of Agricultural and Food Chemistry, 63(11), 2989-2996. https://doi.org/10.1021/acs.ja....
 
32.
Liu, C.J., Lin, J.Y. (2013). Anti-inflammatory effects of phenolic extracts from strawberry and mulberry fruits on cytokine secretion profiles using mouse primary splenocytes and peritoneal macrophages. International Immunopharmacology, 16(2), 165–170. https://doi.org/10.1016/j.inti....
 
33.
Loke, Y.L., Chew, M.T., Ngeow, Y.F., Lim, W.W.D., Peh, S.C. (2020). Colon carcinogenesis: the interplay between diet and gut microbiota. Frontiers in Cellular and Infection Microbiology, 10, art. no. 603086. https://doi.org/10.3389/fcimb.....
 
34.
Lu, Y., Wu, Y., Chen, X., Yang, X., Xiao, H. (2020). Water extract of shepherd's purse prevents high-fructose induced-liver injury by regulating glucolipid metabolism and gut microbiota. Food Chemistry, 16(342), art. no. 128536. https://doi.org/10.1016/j.food....
 
35.
Markowiak-Kopeć, P., Śliżewska, K. (2020). The effect of probiotics on the production of short-chain fatty acids by human intestinal microbiome. Nutrients, 12(4), art. no. 1107. https://doi.org/10.3390/nu1204....
 
36.
Mazzone, G., Marirosa, T., Nino, R. (2013). Density functional predictions of antioxidant activity and UV spectral features of nasutin a, isonasutin, ellagic acid, and one of its possible derivatives. Journal of Agricultural and Food Chemistry, 61(40), 9650-9657. https://doi.org/10.1021/jf4032....
 
37.
Milala, J., Kosmala, M., Karlińska, E., Juśkiewicz, J., Zduńczyk, Z., Fotschki, B. (2017). Ellagitannins from strawberries with different degree of polymerization showed different metabolism through gastrointestinal tract of rats. Journal of Agricultural and Food Chemistry, 65(49), 10738–10748. https://doi.org/10.1021/acs.ja....
 
38.
Molan, A.L., Liu, Z., Kruger, M. (2010). The ability of blackcurrant extracts to possitively modulate key markers of gastrointestinal function in rats. World Journal of Microbiology and Biotechnology, 26(10), 1735– 1743. https://doi.org/10.1007/s11274....
 
39.
Mizobe, T., Nakajima, Y., Ueno, H., Sessler, D.I. (2006). Fructose administration increases intraoperative core temperature by augmenting both metabolic rate and the vasoconstriction threshold. Anesthesiology, 104(6), 1124–1130. https://doi.org/10.1097/000005....
 
40.
Nowicka, A., Kucharska, A.Z., Sokół-Łętowska, A., Fecka, I. (2019). Comparison of polyphenol content and antioxidant capacity of strawberry fruit from 90 cultivars of Fragariaananassa Duch. Food Chemistry, 270, 32–46. https://doi.org/10.1016/j.food....
 
41.
Park, G., Jung, S., Wellen, K.E., Jang, Ch. (2021). The interaction between the gut microbiota and dietary carbohydrates in nonalcoholic fatty liver disease. Experimental & Molecular Medicine, 53, 809–822. https://doi.org/10.1038/s12276....
 
42.
Prior, R.L., Wu, X., Gu, L., Hager, T., Hager, A., Wilkes, S., Howard, L. (2009). Purified berry anthocyanins but not whole berries normalize lipid parameters in mice fed an obesogenic high fat diet. Molecular Nutrition and Food Research, 53(11), 1406-1418. https://doi.org/10.1002/mnfr.2....
 
43.
Rahman, I., Kode, A., Biswas, S.K. (2006). Assay for quantitative determination of glutathione and glutathione disulfide levels using enzymatic recycling method. Nature Protocols, 1(6), 3159-3165. https://doi.org/10.1038/nprot.....
 
44.
Reagan-Shaw, S., Nihal, M., Ahmad, N. (2008.) Dose translation from animal to human studies revisited. The FASEB Journal, 22(3), 659-661. https://doi.org/10.1096/fj.07-....
 
45.
Reeves, P.G. (1997). Components of the AIN-93 diets as improvements in the AIN-76A diet. Journal of Nutrition, 127(5), 838S-841S. https://doi.org/10.1093/jn/127....
 
46.
Selma, M.V., Beltrán, D., García-Villalba, R., Espín, J.C., Tomás-Barberán, F.A. (2014). Description of urolithin production capacity from ellagic acid of two human intestinal Gordonibacter species. Food and Function, 5(8), 1779-1784. https://doi.org/10.1039/C4FO00....
 
47.
Sirijan, M., Pipattanawong, N., Saeng-on, B., Chaiprasart, P. (2020). Anthocyanin content, bioactive compounds and physico-chemical characteristics of potential new strawberry cultivars rich in-anthocyanins. Journal of Berry Research, 10(3), 397-410. https://doi.org/10.3233/JBR190....
 
48.
Sójka, M., Klimczak, E., Macierzyński, J., Kołodziejczyk, K. (2013). Nutrient and polyphenolic composition of industrial strawberry press cake. European Food Research and Technology, 237(6), 995-1007. https://doi.org/10.1007/s00217....
 
49.
Stanisławska, I.J., Granica, S., Piwowarski, J.P., Szawkało, J., Wiązecki, K., Czarnocki, Z., Kiss A.K. (2016). 5-(3',4',5'-trihydroxyphenyl)-γ-valerolactone and nasutin A inhibit LNCaP prostate cancer cell proliferation. Planta Medica, 82(S01), S1-S381. https://doi.org/10.1055/s-0036....
 
50.
Tappy, L., Lê, K.A., (2010). Metabolic effects of fructose and the worldwide increase in obesity. Physiological Reviews, 90(1), 23– 46. https://doi.org/10.1152/physre....
 
51.
Wang, Ch., Wang, X., Song, G., Xing, H., Linquan, Y., Han, K., Chang, Y-Z. (2021). A high‐fructose diet in rats induces systemic iron deficiency and hepatic iron overload by an inflammation mechanism. Journal of Food Biochemistry, 45(1), art. no. e13578. https://doi.org/10.1111/jfbc.1....
 
52.
Xu, J., Yuan, Ch., Wang, G., Ma, H., Jiaming L., Xu, L., Li, L., Seeram N.P., Huang X., Mu, Y., Li, Y. (2018). Urolithins attenuate LPS-induced neuroinflammation in BV2Microglia via MAPK, Akt, and NF-κB signaling pathways. Journal of Agricultural and Food Chemistry, 66(3), 571-580. https://doi.org/10.1021/acs.ja....
 
53.
Zduńczyk, Z., Juśkiewicz, J., Estrella, I. (2006). Caecal parameters of rats fed diets containing grapefruit polyphenols and inulin as single supplements or in a combination. Nutrition, 22(9), 898–904. https://doi.org/10.1016/j.nut.....
 
54.
Zhao, M., Liu, X., Luo, Y., Guo, H., Hu, X., Chen, F. (2015). Evaluation of protective effect of freeze-dried strawberry, grape, and blueberry powder on acrylamide toxicity in mice. Journal of Science, 80(4), H869–H874. https://doi.org/10.1111/1750-3....
 
55.
Żary-Sikorska, E., Fotschki, B., Fotschki, J., Wiczkowski, W., Juśkiewicz, J. (2019). Preparations from purple carrots containing anthocyanins improved intestine microbial activity, serum lipid profile and antioxidant status in rats. Journal of Functional Foods, 60, art. no. 103442. https://doi.org/10.1016/j.jff.....
 
56.
Żary-Sikorska, E., Fotschki, B., Jurgoński, A., Kosmala, M., Milala, J., Kołodziejczyk, K., Majewski, M., Ognik, K., Juśkiewicz, J. (2020). Protective effects of a strawberry ellagitannin-rich extract against pro-oxidative and pro-inflammatory dysfunctions induced by a high-fat diet in a rat model. Molecules, 25(24), art. no. 5874. https://doi.org/10.3390/molecu....
 
 
CITATIONS (7):
1.
Stimulation of the intestinal microbiota with prebiotics enhances hepatic levels of dietary polyphenolic compounds, lipid metabolism and antioxidant status in healthy rats
Bartosz Fotschki, Wiesław Wiczkowski, Tomasz Sawicki, Michał Sójka, Kamil Myszczyński, Katarzyna Ognik, Jerzy Juśkiewicz
Food Research International
 
2.
Gastrointestinal tract and neuroendocrine system responses of young turkeys to the early administration of antibiotics or feeding a diet containing a coccidiostat
Dariusz Mikulski, Jerzy Juśkiewicz, Katarzyna Ognik, Przemysław Zduńczyk, Radosław Smagieł, Jan Jankowski
Poultry Science
 
3.
Jamun Seed: A Review on Bioactive Constituents, Nutritional Value and Health Benefits
Yamini Tak, Manpreet Kaur, Mool Jain, Mahesh Samota, Nirmal Meena, Gurpreet Kaur, Rajendra Kumar, Daisy Sharma, José Lorenzo, Ryszard Amarowicz
Polish Journal of Food and Nutrition Sciences
 
4.
Effect of Chromium Picolinate and Chromium Nanoparticles Added to Low- or High-Fat Diets on Chromium Biodistribution and the Blood Level of Selected Minerals in Rats
Anna Stępniowska, Jerzy Juśkiewicz, Krzysztof Tutaj, Joanna Fotschki, Bartosz Fotschki, Katarzyna Ognik
Polish Journal of Food and Nutrition Sciences
 
5.
Performance indicators, coccidia oocyst counts, plasma biochemical parameters and fermentation processes in the cecum of rabbits fed a diet with the addition of black cumin seed meal
Janusz Strychalski, Dorota Kowalska, Sławomir Grinholc, Jerzy Juśkiewicz, Bartosz Fotschki, Andrzej Gugołek
Annals of Animal Science
 
6.
The Role of Anthocyanins in Alleviating Intestinal Diseases: A Mini Review
Yang Liu, Iva Fernandes, Nuno Mateus, Hélder Oliveira, Fuliang Han
Journal of Agricultural and Food Chemistry
 
7.
Current Perspective About the Effect of a Ketogenic Diet on Oxidative Stress – a Review
Natalia Drabińska
Polish Journal of Food and Nutrition Sciences
 
eISSN:2083-6007
ISSN:1230-0322
Journals System - logo
Scroll to top