Antioxidant and Anticancer Properties of Leaf and Fruit Extracts of the Wild Raspberry (Rubus idaeus L.)

Authors

  • Bojana VELJKOVIC State University of Novi Pazar, Department of Biomedical Sciences, Vuka Karadžića bb, 36300 Novi Pazar (RS)
  • Natasa DJORDJEVIC State University of Novi Pazar, Department of Biomedical Sciences, Vuka Karadžića bb, 36300 Novi Pazar (RS)
  • Zana DOLICANIN State University of Novi Pazar, Department of Biomedical Sciences, Vuka Karadžića bb, 36300 Novi Pazar (RS)
  • Braho LICINA State University of Novi Pazar, Department of Biomedical Sciences, Vuka Karadžića bb, 36300 Novi Pazar (RS)
  • Marina TOPUZOVIC University of Kragujevac, Faculty of Sciences, Institute for Biology and Ecology, Radoja Domanovića 12, 34000 Kragujevac (RS)
  • Milan STANKOVIC University of Kragujevac, Faculty of Sciences, Institute for Biology and Ecology, Radoja Domanovića 12, 34000 Kragujevac (RS)
  • Nenad ZLATIC University of Kragujevac, Faculty of Sciences, Institute for Biology and Ecology, Radoja Domanovića 12, 34000 Kragujevac (RS)
  • Zora DAJIC-STEVANOVIC University of Belgrade, Department of Agrobotany, Nemanjina 6, 11080 Zemun-Belgrade (RS)

DOI:

https://doi.org/10.15835/nbha47111274

Keywords:

biological activity; methanolic extracts; phytochemical analysis; secondary metabolites

Abstract

In this study the leaves and fruits of wild raspberry (Rubus idaeus L.) populations from the central Balkan region were examined to determine the level of secondary metabolites and related antioxidant activity, as well as biological activity, upon existing ethnobotanical evidence, primarily linked to gastrointestinal disorders. The values obtained for total phenols ranged from 59.68 to 96.83 mg GA g-1 and 24.29 to 38.71 mg GA g-1 in leaf and fruit extracts, respectively. The highest values of tannins and anthocyanins were determined for leaf extracts from a population of east Serbia at a level of 1.27 mg mL-1 and 9.00 mg mL-1. Antioxidant activity was evaluated by measuring the scavenging capacity of the extracts on DPPH. Higher antioxidant activity was detected in the leaf extracts than in the fruit extracts. Leaf and fruit extract were the most effective against Escherichia coli (ATCC 8739). Anticancer activity was studied on a human colorectal cancer cell line HCT-116. Leaf extracts exhibited anticancer activity with IC50/24 h 162.38 μg mL-1 and IC50/48 h 95.69 μg mL-1. Wild raspberry leaf and fruit extracts contain numerous secondary metabolites providing marked antioxidant, antimicrobial and anticancer activity.

References

Baby B, Antony P, Vijayan R (2017). Antioxidant and anticancer properties of berries. Critical Reviews in Food Science and Nutrition 1-17. https://doi.org/10.1080/10408398.2017.1329198.

Beekwilder J, Jonker H, Meesters P, Hall RD, van der Meer IM, Ric de Vos CH (2005). Antioxidants in raspberry: on-line analysis links antioxidant activity to a diversity of individual metabolites. Journal of Agricultural and Food Chemistry 53(9):3313-3320.

Benvenuti S, Pellati F, Melegari MA, Bertelli D (2004). Polyphenols, anthocyanins, ascorbic acid, and radical scavenging activity of Rubus, Ribes, and Aronia. Journal of Food Science 69(3):164-169.

Bobinaite R, Viskelis P, Venskutonis PR (2012). Variation of total phenolics, anthocyanins, ellagic acid and radical scavenging capacity in various raspberry (Rubus spp.) cultivars. Food Chemistry 132:1495-1501.

Boivin D, Blanchette M, Barrette S, Moghrabi A, Beliveau R (2007). Inhibition of cancer cell proliferation and suppression of TNF-induced activation of NF?B by edible berry juice. Anticancer Research 27(2):937-948.

Bowen-Forbes CS, Zhang Y, Nair MG (2012). Anthocyanin content, antioxidant, anti-inflammatory and anticancer properties of blackberry and raspberry fruits. Journal of Food Composition and Analysis 23(6):554-560.

Burdulis D, Sarkinas A, Jasutiene I, Stackevicene E, Nikolajevas L, Janulis V (2009). Comparative study of anthocyanin composition, antimicrobial and antioxidant activity in bilberry (Vaccinium myrtillus L.) and blueberry (Vaccinium corymbosum L.) fruits. Acta Poloniae Pharmaceutica 66(4):399-408.

Cao G, Sofic E, Prior RL (1997). Antioxidant and prooxidant behavior of flavonoids: structure-activity relationships. Free Radical Biology and Medicine 22(5):749-760.

Castillo NR (2006). Fingerprinting and genetic stability of Rubus using molecular markers. PhD Thesis, Oregon State University, The USA.

Çekic C, Özgen M (2010). Comparison of antioxidant capacity and phytochemical properties of wild and cultivated red raspberries (Rubus idaeus L.). Journal of Food Composition and Analysis 23(6):540-544.

da Silva FL, Escribano-Bailón MT, Alonso JJ, Rivas-Gonzalo JC, Santos-Buelga C (2007). Anthocyanin pigments in strawberry. LWT - Food Science and Technology 40(2):374-382.

Dujmovic Purgar D, Duralija B, Voca S, Vokurka A, Ercisli S (2012). A comparison of fruit chemical characteristics of two wild grown Rubus species from different locations of Croatia. Molecules 17(9):10390-10398.

Durgo K, Belscak-Cvitanovic A, Stancic A, Franekic J, Komes D (2012). The bioactive potential of red raspberry (Rubus idaeus L.) leaves in exhibiting cytotoxic and cytoprotective activity on human laryngeal carcinoma and colon adenocarcinoma. Journal of Medicinal Food 15(3):258-68.

Duval B, Shetty K, Thomas WH (1999). Phenolic compounds and antioxidant properties in the snow alga Chlamydomonas nivalis after exposure to UV light. Journal of Applied Phycology 11(6):559-566.

Ghasemi K, Ghasemi Y, Ehteshamnia A, Nabavi SM, Nabavi SF, Ebrahimzadeh M A, Pourmorad F (2011). Influence of environmental factors on antioxidant activity, phenol and flavonoids contents of walnut (Juglans regia L.) green husks. Journal of Medicinal Plants Research 5(7):1128-1133.

Gramza-Michalowska A, Sidor A, Kulczynski B (2017). Berries as a potential anti-influenza factor – A review. Journal of Functional Foods 37:116-137.

Gudej J, Tomczyk M (2004). Determination of flavonoids, tannins and ellagic acid in leaves from Rubus L. species. Archives of Pharmacal Research 27(11):1114-1119.

Gülcin ?, Topal F, Çakmakci R, Bilsel M, Gören AC, Erdogan U (2011). Pomological features, nutritional quality, polyphenol content analysis, and antioxidant properties of domesticated and 3 wild ecotype forms of raspberries (Rubus idaeus L.). Journal of Food Science 76(4):585-593.

Holst L, Haavik S, Nordeng H (2004). Raspberry leaf – Should it be recommended to pregnant women? Complementary Therapies in Clinical Practice 15(4):204-208.

Hosu A, Cristea VM, Cimpoiu C (2014). Analysis of total phenolic, flavonoids, anthocyanins and tannins content in Romanian red wines: Prediction of antioxidant activities and classification of wines using artificial neural networks. Food Chemistry 150:113-118.

Huang WY, Cai YZ, Zhang Y. Natural phenolic compounds from medicinal herbs and dietary plants: potential use for cancer prevention. Nutrition and Cancer 62(1):1-20.

Jakobek L, Seruga M, Seruga B, Novak I, Medvidovic-Kosanovic M (2009). Phenolic compound composition and antioxidant activity of fruits of Rubus and Prunus species from Croatia. International Journal of Food Science and Technology 44: 860-868.

Kadoma Y, Fujisawa S (2008). A comparative study of the radical-scavenging activity of the phenolcarboxylic acids caffeic acid, p-coumaric acid, chlorogenic acid and ferulic acid, with or without 2-mercaptoethanol, a thiol, using the induction period method. Molecules 13: 2488-2499.

Khan MM, Haileselassie Y, Navis M, Cooper C, Sverremark-Ekström E, Nilsson AS (2017). Corrigendum: Morphologically distinct Escherichia coli bacteriophages differ in their efficacy and ability to stimulate cytokine release in vitro. Front Microbiology 7:2145.

Kong JM, Chia LS, Goh NK, Chia TF, Brouillard R (2003). Analysis and biological activities of anthocyanins. Phytochemistry 64(5):923-933.

Konic-Ristic A, Šavikin K, Zdunic G, Jankovic T, Juranic Z, Menkovic N, Stankovic I (2011). Biological activity and chemical composition of different berry juices. Food Chemistry 125:1412-1417.

Lam-Himlin D, Montgomery E, Torbenson M (2012). Non-neoplastic and neoplastic disorders of the appendix. Gastrointestinal and Liver Pathology 2:257-296.

Liu CH, Chiu CH, Wang SW, Cheng W (2012). Dietary administration of the probiotic, Bacillus subtilis E20, enhances the growth, innate immune responses, and disease resistance of the grouper, Epinephelus coioides. Fish Shellfish Immunology 33(4):699-706.

Määttä-Riihinen KR, Kamal-Eldin A, Törrönen AR (2014). Identification and quantification of phenolic compounds in berries of Fragaria and Rubus species (family Rosaceae). Journal of Agricultural and Food Chemistry 52(20):6178-6187.

Marulanda ML, López AM, Aguilar SB (2007). Genetic diversity of wild and cultivated Rubus species in Colombia using AFLP and SSR markers. Crop Breeding and Applied Biotechnology 7(3):242-252.

Menkovic N, Šavikin K, Zdunic G, Milosavljevic S, Živkovic J (2014). Medicinal Plants in Northern Montenegro: Traditional Knowledge, Quality, and Resources. In: Pieroni A, Quave CL (Eds). Ethnobotany and Biocultural Diversities in the Balkans. New York, Springer pp 197-228.

Mikulic-Petkovsek M, Schmitzer V, Slatnar A, Stampar F, Veberic R (2012). Composition of sugars, organic acids, and total phenolics in 25 wild or cultivated berry species. Journal of Food Science 77(10):1064-1070.

Mosmann T (1983). Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. Journal of Immunology Methods 65(1-2):55-63.

Patel AV, Rojas-Vera J, Dacke CG (2004). Therapeutic constituents and actions of Rubus species. Current Medicinal Chemistry 11(11):1501-1512.

Quettier-Deleu C, Gressier B, Vasseur J, Dine T, Brunet C, Luyckx M, Cazin M, Cazin JC, Bailleul F, Trotin F (2000). Phenolic compounds and antioxidant activities of buckwheat (Fagopyrum esculentum Moench) hulls and flour. Journal of Ethnopharmacology 72(1-2):35-42.

Rao AV, Snyder DM (2010). Raspberries and human health: a review. Journal of Agricultural and Food Chemistry 58(7):3871-3883.

Rauha JP, Remes S, Heinonen M, Hopia A, Kähkönen M, Kujala T, Pihlaja K, Vuorela H, Vuorela P (2000). Antimicrobial effects of Finnish plant extracts containing flavonoids and other phenolic compounds. International Journal of Food Microbiology 56(1):3-12.

Rowe B (1979). The role of Escherichia coli in gastroenteritis. Clinics in Gastroenterology 8(3):625-644.

Sarker SD, Nahar L, Kumarasamy Y (2007). Microtitre plate-based antibacterial assay incorporating resazurin as an indicator of cell growth, and its application in the in vitro antibacterial screening of phytochemicals. Methods 42(4):321-324.

Seeram NP, Adams LS, Zhang Y, Lee R, Sand D, Scheuller HS, Heber D (2006). Blackberry, black raspberry, blueberry, cranberry, red raspberry, and strawberry extracts inhibit growth and stimulate apoptosis of human cancer cells in vitro. Journal of Agricultural and Food Chemistry 54(25):9329-9339.

Seeram NP (2008). Berry fruits for cancer prevention: current status and future prospects. Journal of Agricultural and Food Chemistry 56(3):630-635.

Stankovic MS, Petrovic M, Godjevac D, Stevanovic ZD (2015). Screening inland halophytes from the central Balkan for their antioxidant activity in relation to total phenolic compounds and flavonoids: Are there any prospective medicinal plants? Journal of Arid Environments 120:26-32.

Sun J, Kato I (2016). Gut microbiota, inflammation and colorectal cancer. Genes & Diseases 3:130-143.

Takao T, Kitatani F, Watanabe N, Yagi A, Sakata K (1994). A simple screening method for antioxidants and isolation of several antioxidants produced by marine bacteria from fish and shellfish. Bioscience, Biotechnology and Biochemistry 58(10):1780-1783.

Tosun M, Ercisli S, Karlidag H, Sengul M (2009). Characterization of red raspberry (Rubus idaeus L.) genotypes for their physicochemical properties. Journal of Food Sciences 74(7):575-579.

Trivedi AK, Verma SK, Tyagi RK (2016). Variability in morpho-physiological traits and antioxidant potential of Rubus species in Central Himalayan Region. Industrial Crops and Products 82:1-8.

Veberic R, Slatnar A, Bizjak J, Stampar F, Mikulic-Petkovsek M (2015). Anthocyanin composition of different wild and cultivated berry species. LWT - Food Science and Technology 60(1):509-517.

Vyas P, Kalidindi S, Chibrikova L, Igamberdiev AU, Weber JT (2013). Chemical analysis and effect of blueberry and lingonberry fruits and leaves against glutamate-mediated excitotoxicity. Journal of Agricultural and Food Chemistry 61(32):7769-7776.

Wang SY, Lin HS. (2000) Antioxidant activity in fruits and leaves of blackberry, raspberry, and strawberry varies with cultivar and developmental stage. Journal of Agricultural and Food Chemistry 48(2):140-146.

Wootton-Beard PC, Moran A, Ryan L (2011). Stability of the total antioxidant capacity and total polyphenol content of 23 commercially available vegetable juices before and after in vitro digestion measured by FRAP, DPPH, ABTS and Folin - Ciocalteu methods. Food Research International 44(1):217-224.

Downloads

Published

2018-12-21

How to Cite

VELJKOVIC, B., DJORDJEVIC, N., DOLICANIN, Z., LICINA, B., TOPUZOVIC, M., STANKOVIC, M., ZLATIC, N., & DAJIC-STEVANOVIC, Z. (2018). Antioxidant and Anticancer Properties of Leaf and Fruit Extracts of the Wild Raspberry (Rubus idaeus L.). Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 47(2), 359–367. https://doi.org/10.15835/nbha47111274

Issue

Section

Research Articles
CITATION
DOI: 10.15835/nbha47111274