Centaurium erythraea methanol extract protects red blood cells from oxidative damage in streptozotocin-induced diabetic rats

Journal of Ethnopharmacology

Volumn 202, Issue , 2017, Pages 172-183

  Đorđević, Miloš ^a   Mihailović, Mirjana ^a   Arambašić Jovanović, Jelena ^a   Grdović, Nevena ^a   Uskoković, Aleksandra ^a   Tolić, Anja ^a   Sinadinović, Marija ^a   Rajić, Jovana ^a   Mišić, Danijela ^a   Šiler, Branislav ^a   Poznanović, Goran ^a   Vidaković, Melita ^a   Dinić, Svetlana ^a  

^a UNIVERSITY OF BELGRADE   (Serbia)

Author keywords

Antioxidant activity; Centaurium erythraea; Diabetes mellitus; Hyperglycemia; Oxidative stress; Red blood cells

Indexed keywords

ADVANCED GLYCATION END PRODUCT; ALPHA 2 MACROGLOBULIN; ANTIOXIDANT; BIOLOGICAL MARKER; CATALASE; CENTAURIUM ERYTHRAEA EXTRACT; CHOLESTEROL; CYTOPROTECTIVE AGENT; GLUCOSE; GLUTATHIONE DISULFIDE; GLUTATHIONE PEROXIDASE; GLUTATHIONE REDUCTASE; GLYCOSYLATED HEMOGLOBIN; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; INSULIN; LOW DENSITY LIPOPROTEIN CHOLESTEROL; PLANT EXTRACT; PROTEIN KINASE B; STREPTOZOCIN; SUPEROXIDE DISMUTASE; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; ANTIDIABETIC AGENT; FLAVONOID; GLUCOSE BLOOD LEVEL; GLUTATHIONE; METHANOL; PHENOL DERIVATIVE; SCAVENGER;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIDIABETIC ACTIVITY; ANTIOXIDANT ACTIVITY; ARTICLE; CELL PROTECTION; CENTAURIUM; CENTAURIUM ERYTHRAEA; CHEMICAL COMPOSITION; CONTROLLED STUDY; ENZYME ACTIVITY; ERYTHROCYTE; GLUCOSE BLOOD LEVEL; GLYCEMIC CONTROL; HEMOGLOBIN BLOOD LEVEL; INSULIN BLOOD LEVEL; LIPID PEROXIDATION; MALE; NONHUMAN; OXIDATIVE STRESS; PROTEIN AGGREGATION; PROTEIN GLYCOSYLATION; RAT; STREPTOZOTOCIN-INDUCED DIABETES MELLITUS; ANIMAL; BLOOD; CHEMISTRY; DIABETES MELLITUS, EXPERIMENTAL; DRUG EFFECTS; METABOLISM; WISTAR RAT;

ANIMALS; ANTIOXIDANTS; BLOOD GLUCOSE; CENTAURIUM; DIABETES MELLITUS, EXPERIMENTAL; ERYTHROCYTES; FLAVONOIDS; FREE RADICAL SCAVENGERS; GLUTATHIONE; HYPOGLYCEMIC AGENTS; LIPID PEROXIDATION; METHANOL; OXIDATIVE STRESS; PHENOLS; PLANT EXTRACTS; RATS; RATS, WISTAR;

EID: 85015364390     PISSN: 03788741     EISSN: 18727573     Source Type: Journal    
DOI: 10.1016/j.jep.2017.03.016     Document Type: Article

References (90)

1. Adisakwattana, S., Chantarasinlapin, P., Thammarat, H., Yibchok-Anun, S., A series of cinnamic acid derivatives and their inhibitory activity on intestinal alpha-glucosidase. J. Enzyme Inhib. Med. Chem. 24 (2009), 1194–1200.
2. Al-Numair, K.S., Chandramohan, G., Veeramani, C., Alsaif, M.A., Ameliorative effect of kaempferol, a flavonoid, on oxidative stress in streptozotocin-induced diabetic rats. Redox Rep. 20 (2015), 198–209.
3. Bajaj, S., Khan, A., Antioxidants and diabetes. Indian J. Endocrinol. Metab. 16:Suppl 2 (2012), S267–S271.
4. Beckman, J.A., Creager, M.A., Libby, P., Diabetes and atherosclerosis: epidemiology, pathophysiology, and management. JAMA 287 (2002), 2570–2581.
5. Beutler, E., Catalase. Beutler, E., (eds.) Red Cell Metabolism, a Manual of Biochemical Methods, 1982, Grune and Stratton, Inc., New York, 105–106.
6. Blakytny, R., Harding, J.J., Glycation (non-enzymic glycosylation) inactivates glutathione reductase. Biochem J. 288:Pt 1 (1992), 303–307.
7. Blois, M.S., Antioxidant determinations by the use of a stable free radical. Nature 26 (1958), 1199–1200.
8. Brown, G.C., Reversible binding and inhibition of catalase by nitric oxide. Eur. J. Biochem. 232 (1995), 188–191.
9. Brownlee, M., Biochemistry and molecular cell biology of diabetic complications. Nature 414 (2001), 813–820.
10. Bryszewska, M., Zavodnik, I.B., Niekurzak, A., Szosland, K., Oxidative processes in red blood cells from normal and diabetic individuals. Biochem Mol. Biol. Int. 37 (1995), 345–354.
11. Caimi, G., Serra, A., Presti, R.I., Red cell calcium accumulation (total and cytosolic) and erythrocyte membrane fluidity in several clinical conditions. Clin. Hemorheol. 13 (1993), 227–235.
12. Cho, Y.I., Mooney, M.P., Cho, D.J., Hemorheological disorders in diabetes mellitus. J. Diabetes Sci. Technol. 2 (2008), 1130–1138.
13. Choi, J., Kang, H.J., Kim, S.Z., Kwon, T.O., Jeong, S.I., Jang, S.I., Antioxidant effect of astragalin isolated from the leaves of Morus alba L. against free radical-induced oxidative hemolysis of human red blood cells. Arch. Pharm. Res. 36 (2013), 912–917.
14. Chung, S.S., Ho, E.C., Lam, K.S., Chung, S.K., Contribution of polyol pathway to diabetes-induced oxidative stress. J. Am. Soc. Nephrol. 14 (2003), S233–S236.
15. Dallak, M., Jaliah, B.I., Antioxidant activity of Citrullus colocynthis pulp extract in the RBC's of alloxan-induced diabetic rats. Pak. J. Physiol. 6 (2010), 1–5.
16. Djeridane, A., Yousfi, M., Nadjemi, B., Boutassouna, D., Stocker, P., Vidal, N., Antioxidant activity of some algerian medicinal plants extracts containing phenolic compounds. Food Chem. 97 (2006), 654–660.
17. Drabkin, A., Austin, H., Spectrophotometric studies preparations from washed blood cells. J. Biol. Chem. 112 (1935), 51–55.
18. Elbe, H., Vardi, N., Esrefoglu, M., Ates, B., Yologlu, S., Taskapan, C., Amelioration of streptozotocin-induced diabetic nephropathy by melatonin, quercetin, and resveratrol in rats. Hum. Exp. Toxicol. 34 (2015), 100–113.
19. Erlund, I., Meririnne, E., Alfthan, G., Aro, A., Plasma kinetics and urinary excretion of the flavanones naringenin and hesperetin in humans after ingestion of orange juice and grapefruit juice. J. Nutr. 131 (2001), 235–241.
20. Garratt, D.C., The Quantitative Analysis of Drugs. 1964, Chapman and Hall Limited, Tokyo.
21. Glatzle, D., Vuilleumier, J.P., Weber, F., Decker, K., Glutathione reductase test with whole blood, a convenient procedure for the assessment of the riboflavin status in humans. Experientia 30 (1974), 665–667.
22. Halliwell, B., Gutteridge, J.M., Oxygen free radicals and iron in relation to biology and medicine: some problems and concepts. Arch. Biochem. Biophys. 246 (1986), 501–514.
23. Hamza, N., Berke, B., Cheze, C., Agli, A.N., Robinson, P., Gin, H., Moore, N., Prevention of type 2 diabetes induced by high fat diet in the C57BL/6J mouse by two medicinal plants used in traditional treatment of diabetes in the east of Algeria. J. Ethnopharmacol. 128 (2010), 513–518.
24. Hamza, N., Berke, B., Cheze, C., Le Garrec, R., Lassalle, R., Agli, A.N., Robinson, P., Gin, H., Moore, N., Treatment of high fat diet induced type 2 diabetes in C57BL/6J mice by two medicinal plants used in traditional treatment of diabetes in the east of Algeria. J. Ethnopharmacol. 133 (2011), 931–933.
25. Hanhineva, K., Torronen, R., Bondia-Pons, I., Pekkinen, J., Kolehmainen, M., Mykkanen, H., Poutanen, K., Impact of dietary polyphenols on carbohydrate metabolism. Int. J. Mol. Sci. 11 (2010), 1365–1402.
26. Hatjimanoli, M., Debelmas, A.M., Study of Centaurium umbellatum Gil. Identification of phenolic acids. Ann. Pharm. Fr. 35 (1977), 107–111.
27. Huertas, A., Das, S.R., Emin, M., Sun, L., Rifkind, J.M., Bhattacharya, J., Bhattacharya, S., Erythrocytes induce proinflammatory endothelial activation in hypoxia. Am. J. Respir. Cell Mol. Biol. 48 (2013), 78–86.
28. Iwai, K., Antidiabetic and antioxidant effects of polyphenols in brown alga Ecklonia stolonifera in genetically diabetic KK-A(y) mice. Plant Foods Hum. Nutr. 63 (2008), 163–169.
29. Jaishree, V., Badami, S., Antioxidant and hepatoprotective effect of swertiamarin from Enicostemma axillare against D-galactosamine induced acute liver damage in rats. J. Ethnopharmacol. 130 (2010), 103–106.
30. Jarić, S., Macukanović-Jocić, M., Djurdjević, L., Mitrović, M., Kostić, O., Karadžić, B., Pavlović, P., An ethnobotanical survey of traditionally used plants on Suva planina mountain (south-eastern Serbia). J. Ethnopharmacol. 175 (2015), 93–108.
31. Johnston, K., Sharp, P., Clifford, M., Morgan, L., Dietary polyphenols decrease glucose uptake by human intestinal Caco-2 cells. FEBS Lett. 579 (2005), 1653–1657.
32. Jung, E.H., Kim, S.R., Hwang, I.K., Ha, T.Y., Hypoglycemic effects of a phenolic acid fraction of rice bran and ferulic acid in C57BL/KsJ-db/db mice. J. Agric. Food Chem. 55 (2007), 9800–9804.
33. Jung, H.A., Su, B.N., Keller, W.J., Mehta, R.G., Kinghorn, A.D., Antioxidant xanthones from the pericarp of Garcinia mangostana (Mangosteen). J. Agric. Food Chem. 54 (2006), 2077–2082.
34. Kalousova, M., Skrha, J., Zima, T., Advanced glycation end-products and advanced oxidation protein products in patients with diabetes mellitus. Physiol. Res. 51 (2002), 597–604.
35. Kobayashi, Y., Suzuki, M., Satsu, H., Arai, S., Hara, Y., Suzuki, K., Miyamoto, Y., Shimizu, M., Green tea polyphenols inhibit the sodium-dependent glucose transporter of intestinal epithelial cells by a competitive mechanism. J. Agric. Food Chem. 48 (2000), 5618–5623.
36. Li, J.M., Che, C.T., Lau, C.B., Leung, P.S., Cheng, C.H., Inhibition of intestinal and renal Na+-glucose cotransporter by naringenin. Int. J. Biochem. Cell Biol. 38 (2006), 985–995.
37. Li, R., Yuan, C., Dong, C., Shuang, S., Choi, M.M., In vivo antioxidative effect of isoquercitrin on cadmium-induced oxidative damage to mouse liver and kidney. Naunyn Schmiede. Arch. Pharmacol. 383 (2011), 437–445.
38. Li, S.Y., Sigmon, V.K., Babcock, S.A., Ren, J., Advanced glycation endproduct induces ROS accumulation, apoptosis, MAP kinase activation and nuclear O-GlcNAcylation in human cardiac myocytes. Life Sci. 80 (2007), 1051–1056.
39. Maiese, K., Morhan, S.D., Chong, Z.Z., Oxidative stress biology and cell injury during type 1 and type 2 diabetes mellitus. Curr. Neurovasc. Res. 4 (2007), 63–71.
40. Maqsood, S., Benjakul, S., Abushelaibi, A., Alam, A., Phenolic compounds and plant phenolic extracts as natural antioxidants in prevention of lipid oxidation in seafood: a detailed review. Compr. Rev. Food Sci. Food Saf. 13 (2014), 1125–1140.
41. Maritim, A.C., Sanders, R.A., Watkins, J.B. 3rd, Diabetes, oxidative stress, and antioxidants: a review. J. Biochem. Mol. Toxicol. 17 (2003), 24–38.
42. Martinez, A., Hernandez-Marin, E., Galano, A., Xanthones as antioxidants: a theoretical study on the thermodynamics and kinetics of the single electron transfer mechanism. Food Funct. 3 (2012), 442–450.
43. Mihailović, M., Arambašić, J., Uskoković, A., Dinić, S., Grdović, N., Marković, J., Poznanović, G., Vidaković, M., Alpha-lipoic acid preserves the structural and functional integrity of red blood cells by adjusting the redox disturbance and decreasing O-GlcNAc modifications of antioxidant enzymes and heat shock proteins in diabetic rats. Eur. J. Nutr. 51 (2012), 975–986.
44. Mišić, D., Šiler, B., Gašić, U., Avramov, S., Živković, S., Nestorović Živković, J., Milutinović, M., Tešić, Ž., Simultaneous UHPLC/DAD/(+/)HESI–MS/MS analysis of phenolic acids and nepetalactones in methanol extracts of Nepeta species: a possible application in chemotaxonomic studies. Phytochem. Anal. 26 (2015), 72–85.
45. Misra, H.P., Fridovich, I., The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. J. Biol. Chem. 247 (1972), 3170–3175.
46. Mohamed, J., Shing, S.W., Idris, M.H., Budin, S.B., Zainalabidin, S., The protective effect of aqueous extracts of roselle (Hibiscus sabdariffa L. UKMR-2) against red blood cell membrane oxidative stress in rats with streptozotocin-induced diabetes. Clinics 68 (2013), 1358–1363.
47. Mohanty, J.G., Nagababu, E., Rifkind, J.M., Red blood cell oxidative stress impairs oxygen delivery and induces red blood cell aging. Front Physiol., 5, 2014, 84.
48. Nagababu, E., Rifkind, J.M., Reaction of hydrogen peroxide with ferrylhemoglobin: superoxide production and heme degradation. Biochemistry 39 (2000), 12503–12511.
49. Nair, A.B., Jacob, S., A simple practice guide for dose conversion between animals and human. J. Basic Clin. Pharm. 7 (2016), 27–31.
50. Navarro-Nunez, L., Lozano, M.L., Palomo, M., Martinez, C., Vicente, V., Castillo, J., Benavente-Garcia, O., Diaz-Ricart, M., Escolar, G., Rivera, J., Apigenin inhibits platelet adhesion and thrombus formation and synergizes with aspirin in the suppression of the arachidonic acid pathway. J. Agric. Food Chem. 56 (2008), 2970–2976.
51. Nawale, R.B., Mourya, V.K., Bhise, S.B., Non-enzymatic glycation of proteins: a cause for complications in diabetes. Indian J. Biochem. Biophys. 43 (2006), 337–344.
52. Nićiforović, N., Abramovič, H., Sinapic acid and its derivatives: natural sources and bioactivity. Compr. Rev. Food Sci. Food Saf. 13 (2014), 34–51.
53. Noh, H., King, G.L., The role of protein kinase C activation in diabetic nephropathy. Kidney Int. Suppl., 2007, S49–S53.
54. O'Brien, B.A., Harmon, B.V., Cameron, D.P., Allan, D.J., Beta-cell apoptosis is responsible for the development of IDDM in the multiple low-dose streptozotocin model. J. Pathol. 178 (1996), 176–181.
55. Ohkawa, H., Ohishi, N., Yagi, K., Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal. Biochem 95 (1979), 351–358.
56. Oyaizu, M., Studies on product of browning reaction prepared from glucose amine. Jpn. J. Nutr. 44 (1986), 307–315.
57. Ozkol, H., Tuluce, Y., Dilsiz, N., Koyuncu, I., Therapeutic potential of some plant extracts used in Turkish traditional medicine on streptozocin-induced type 1 diabetes mellitus in rats. J. Membr. Biol. 246 (2013), 47–55.
58. Parker, K.M., England, J.D., Da Costa, J., Hess, R.L., Goldstein, D.E., Improved colorimetric assay for glycosylated hemoglobin. Clin. Chem. 27 (1981), 669–672.
59. Radović, M., Šiler, B., Nestorović Živković, J., Banjanac, T., Živković, S., Soković, M., Mišić, D., Bioreactor cultivation of Zeltnera beyrichii (Torr. & A. gray) mans.: a novel source of biologically active compounds. Rec. Nat. Prod. 7 (2013), 266–280.
60. Ramkumar, K.M., Vijayakumar, R.S., Vanitha, P., Suganya, N., Manjula, C., Rajaguru, P., Sivasubramanian, S., Gunasekaran, P., Protective effect of gallic acid on alloxan-induced oxidative stress and osmotic fragility in rats. Hum. Exp. Toxicol. 33 (2014), 638–649.
61. Rizvi, S.I., Zaid, M.A., Anis, R., Mishra, N., Protective role of tea catechins against oxidation-induced damage of type 2 diabetic erythrocytes. Clin. Exp. Pharmacol. Physiol. 32 (2005), 70–75.
62. Rohn, T.T., Nelson, L.K., Waeg, G., Quinn, M.T., U-101033E (2,4-diaminopyrrolopyrimidine), a potent inhibitor of membrane lipid peroxidation as assessed by the production of 4-hydroxynonenal, malondialdehyde, and 4-hydroxynonenal—protein adducts. Biochem. Pharmacol. 56 (1998), 1371–1379.
63. Romanova, D., Vachalkova, A., Cipak, L., Ovesna, Z., Rauko, P., Study of antioxidant effect of apigenin, luteolin and quercetin by DNA protective method. Neoplasma 48 (2001), 104–107.
64. Roy, S., Metya, S.K., Sannigrahi, S., Rahaman, N., Ahmed, F., Treatment with ferulic acid to rats with streptozotocin-induced diabetes: effects on oxidative stress, pro-inflammatory cytokines, and apoptosis in the pancreatic beta cell. Endocrine 44 (2013), 369–379.
65. Ruch, R.J., Cheng, S.J., Klaunig, J.E., Prevention of cytotoxicity and inhibition of intracellular communication by antioxidant catechins isolated from Chinese green tea. Carcinogenesis 10 (1989), 1003–1008.
66. Saleh, J., Glycated hemoglobin and its spinoffs: cardiovascular disease markers or risk factors*. World J. Cardiol. 7 (2015), 449–453.
67. Sefi, M., Fetoui, H., Lachkar, N., Tahraoui, A., Lyoussi, B., Boudawara, T., Zeghal, N., Centaurium erythrea (Gentianaceae) leaf extract alleviates streptozotocin-induced oxidative stress and beta-cell damage in rat pancreas. J. Ethnopharmacol. 135 (2011), 243–250.
68. Sen, S., Kar, M., Roy, A., Chakraborti, A.S., Effect of nonenzymatic glycation on functional and structural properties of hemoglobin. Biophys. Chem. 113 (2005), 289–298.
69. Šiler, B., Živković, S., Banjanac, T., Cvetković, J., Nestorović Živković, J., Ćirić, A., Soković, M., Mišić, D., Centauries as underestimated food additives: antioxidant and antimicrobial potential. Food Chem. 147 (2014), 367–376.
70. Singh, M., Shin, S., Changes in erythrocyte aggregation and deformability in diabetes mellitus: a brief review. Indian J. Exp. Biol. 47 (2009), 7–15.
71. Singleton, V.L., Rossi, J.A.J., Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. Am. J. Enol. Vitic. 16 (1965), 144–158.
72. Sivilotti, M.L., Oxidant stress and haemolysis of the human erythrocyte. Toxicol. Rev. 23 (2004), 169–188.
73. Stefkov, G., Miova, B., Dinevska-Kjovkarovska, S., Stanoeva, J.P., Stefova, M., Petrusevska, G., Kulevanova, S., Chemical characterization of Centaurium erythrea L. and its effects on carbohydrate and lipid metabolism in experimental diabetes. J. Ethnopharmacol. 152 (2014), 71–77.
74. Suhr, F., Brenig, J., Muller, R., Behrens, H., Bloch, W., Grau, M., Moderate exercise promotes human RBC-NOS activity, NO production and deformability through Akt kinase pathway. PLoS One, 7, 2012, e45982.
75. Sureka, C., Ramesh, T., Begum, V.H., Attenuation of erythrocyte membrane oxidative stress by Sesbania grandiflora in streptozotocin-induced diabetic rats. Biochem. Cell Biol. 93 (2015), 385–395.
76. Tadera, K., Minami, Y., Takamatsu, K., Matsuoka, T., Inhibition of alpha-glucosidase and alpha-amylase by flavonoids. J. Nutr. Sci. Vitam. 52 (2006), 149–153.
77. Tamura, M., Oshino, N., Chance, B., Some characteristics of hydrogen- and alkylhydroperoxides metabolizing systems in cardiac tissue. J. Biochem. 92 (1982), 1019–1031.
78. Teixeira, J., Gaspar, A., Garrido, E.M., Garrido, J., Borges, F., Hydroxycinnamic acid antioxidants: an electrochemical overview. Biomed. Res. Int., 2013, 2013, 251754.
79. Telci, A., Cakatay, U., Kayali, R., Erdogan, C., Orhan, Y., Sivas, A., Akcay, T., Oxidative protein damage in plasma of type 2 diabetic patients. Horm. Metab. Res. 32 (2000), 40–43.
80. Torregiani, F., Umansky-Zeverin, M., Riqueline, B., Rasia, R., Hemorheological alterations in diabetic patients. Clin. Hemorheol. 15 (1995), 678–690.
81. Tu, H., Li, H., Wang, Y., Niyyati, M., Leshin, J., Levine, M., Low red blood cell vitamin C concentrations induce red blood cell fragility: a link to diabetes via glucose, glucose transporters, and dehydroascorbic acid. EBioMedicine 2 (2015), 1735–1750.
82. Vaidya, H., Prajapati, A., Rajani, M., Sudarsanam, V., Padh, H., Goyal, R.K., Beneficial effects of swertiamarin on dyslipidaemia in streptozotocin-induced type 2 diabetic rats. Phytother. Res. 26 (2012), 1259–1261.
83. Valentao, P., Fernandes, E., Carvalho, F., Andrade, P.B., Seabra, R.M., Bastos, M.L., Antioxidant activity of Centaurium erythraea infusion evidenced by its superoxide radical scavenging and xanthine oxidase inhibitory activity. J. Agric. Food Chem. 49 (2001), 3476–3479.
84. Valentova, K., Vrba, J., Bancirova, M., Ulrichova, J., Kren, V., Isoquercitrin: pharmacology, toxicology, and metabolism. Food Chem. Toxicol. 68 (2014), 267–282.
85. Wang, Y.B., Ge, Z.M., Kang, W.Q., Lian, Z.X., Yao, J., Zhou, C.Y., Rutin alleviates diabetic cardiomyopathy in a rat model of type 2 diabetes. Exp. Ther. Med. 9 (2015), 451–455.
86. Welsch, C.A., Lachance, P.A., Wasserman, B.P., Dietary phenolic compounds: inhibition of Na+-dependent D-glucose uptake in rat intestinal brush border membrane vesicles. J. Nutr. 119 (1989), 1698–1704.
87. Wolffenbuttel, B.H., Giordano, D., Founds, H.W., Bucala, R., Long-term assessment of glucose control by haemoglobin-AGE measurement. Lancet 347 (1996), 513–515.
88. Yan, H., Harding, J.J., Glycation-induced inactivation and loss of antigenicity of catalase and superoxide dismutase. Biochem. J. 328:Pt 2 (1997), 599–605.
89. Yanagisawa, K., Makita, Z., Shiroshita, K., Ueda, T., Fusegawa, T., Kuwajima, S., Takeuchi, M., Koike, T., Specific fluorescence assay for advanced glycation end products in blood and urine of diabetic patients. Metabolism 47 (1998), 1348–1353.
90. Zlatković, B.K., Bogosavljević, S.S., Radivojević, A.R., Pavlović, M.A., Traditional use of the native medicinal plant resource of Mt. Rtanj (Eastern Serbia): ethnobotanical evaluation and comparison. J. Ethnopharmacol. 151 (2014), 704–713.