Journal of Food Measurement and Characterization

, Volume 13, Issue 3, pp 2062–2074 | Cite as

Sage (Salvia pilifera): determination of its polyphenol contents, anticholinergic, antidiabetic and antioxidant activities

  • İlhami GülçinEmail author
  • Ahmet Zafer Tel
  • Ahmet C. Gören
  • Parham Taslimi
  • Saleh H. Alwasel
Original Paper


In this work, we determined for the first time the Salvia pilifera Montbret & Aucher ex Bentham as an important source for natural products with antioxidant and antidiabetic potentials. In this context, methanol (MESP) and water (WESP) extracts were prepared from aerial parts of S. pilifera. Also, it was evaluated for antioxidant profile by eight distinguishes bioanalytical methods and inhibition effects against enzymes linked to different diseases, namely butyrylcholinesterase (BChE), acetylcholinesterase (AChE), α-glycosidase and α-amylase. Also, the polyphenolic compositions of MESP and WESP were evaluated by high performance liquid chromatography and tandem mass spectrometry (LC–MS/MS). Fourteen phenolics were identified in the evaporated MESP and thirteen phenolic compounds were identified in the lyophilized WESP. Also, we performed the antioxidant properties of both extracts. In order to estimate the capacity of MESP and WESP to act as antioxidants, 1,1-diphenyl-2-picryl-hydrazyl radicals (DPPH·), 2,2´-azino-bis(3-ethylbenzthiazoline-6-sulfonic acid) radicals (ABTS·+) and N,N-dimethyl-p-phenylenediamine radicals (DMPD·+), scavenging activities, ferric ions (Fe3+), Fe3+-TPTZ and cupric ions (Cu2+) reducing assays were studied. MESP and WESP were found as potent effective DPPH· (IC50: 7.05 and 8.56 μg/mL), ABTS·+ (IC50: 3.52 and 4.76 μg/mL) and DMPD·+ (IC50: 28.92 and 30.95 μg/mL) scavenging effects. On the other hand, MESP and WESP showed the potent inhibition effects against AChE (IC50: 94.93 and 138.61 μg/mL), BChE (IC50: 60.05 and 99.13 μg/mL), α-glycosidase (IC50: 23.28 and 36.47 μg/mL) and α-amylase (IC50: 46.21 and 97.67 μg/mL) enzymes. This study will be an innovative and guider for further studies for antioxidant properties for industrial or medicinal plants.


Salvia pilifera Antioxidant activity Polyphenol content Enzyme inhibition LC–MS/MS 



S.A. would like to extend his sincere appreciation to the Distinguished Scientist Fellowship Program at King Saud University for funding this research.

Compliance with ethical standards

Conflict of interest

The authors report no conflict of interests.


  1. 1.
    M.J. Rodrigues, C.A. Pereira, M. Oliveira, N.R. Neng, J.M.F. Nogueir, G. Zengin, M.F. Mahomoodallyd, L. Custodio, Ind. Crops Prod. 121, 250–257 (2018)CrossRefGoogle Scholar
  2. 2.
    M. Elmastas, S.M. Celik, N. Genc, H. Aksit, R. Erenler, İ. Gulçin, Int. J. Food Prop. 21, 374–384 (2018)CrossRefGoogle Scholar
  3. 3.
    A. Dalar, M. Mukemre, M. Unal, F. Ozgokce, J. Ethnopharmacol. 226, 56–72 (2018)CrossRefPubMedGoogle Scholar
  4. 4.
    M. Coşkun, A.M. Gençler-Özkan, Phytochemistry 66, 956–960 (2005)CrossRefPubMedGoogle Scholar
  5. 5.
    J.J. Villaverde, P. Sandín-españa, B. Sevilla-morán, C. López-goti, J.L. Alonso-prados, BioResource 11, 5618–5640 (2016)CrossRefGoogle Scholar
  6. 6.
    M.F. Mahomoodally, S. Vlaisavljevic, S. Berezni, H.H. Abdallah, G. Zengine, A.G. Atanasov, A. Mollica, D. Lobine, A. Aktumsek, Ind. Crops Prod. 120, 270–278 (2018)CrossRefGoogle Scholar
  7. 7.
    G. Zengin, Z. Aumeeruddy-Elalfi, A. Mollica, M.A. Yilmaz, M.F. Mahomoodally, Phytomedicine 38, 35–44 (2018)CrossRefPubMedGoogle Scholar
  8. 8.
    M. Sharifi-Rad, B. Ozcelik, G. Altın, C. Daşkaya-Dikmen, M. Martorell, K. Ramírez-Alarcón, P. Alarcón-Zapata, M.F.B. Morais-Braga, J.N.P. Carneiro, A.L.A.B. Leal, H.D.M. Coutinho, R. Gyawali, R. Tahergorabi, S.A.I.R. Sahrifi-Rad, F. Sharopov, B. Saleh, M. del Mar Contreras, A. Segura-Carretero, S. Sen, K. Acharya, J. Sharifi-Rad, Trends Food Sci. Technol. 80, 242–263 (2018)CrossRefGoogle Scholar
  9. 9.
    I.E. Orhan, F.S. Senol, N. Ozturk, G. Akaydin, B. Sener, Food Chem. 132, 1360–1367 (2012)CrossRefPubMedGoogle Scholar
  10. 10.
    C. Franz, J. Novak, in Handbook of Essential Oils, Science, Technology, vol. 994, ed. by K.H.C. Baser, G. Buchbauer (CRC Press, London, 2010)Google Scholar
  11. 11.
    P. Taslimi, I. Gulcin, J. Food Biochem. 42(3), e12516 (2018)CrossRefGoogle Scholar
  12. 12.
    I. Gulcin, R. Elias, A. Gepdiremen, L. Boyer, Eur. Food Res. Technol. 223, 759–767 (2006)CrossRefGoogle Scholar
  13. 13.
    M. Elmastas, I. Gulcin, Ö. Işıldak, Öİ. Küfrevioğlu, K. İbaoğlu, H.Y. Aboul-Enein, J. Iran. Chem. Soc. 3(3), 258–266 (2006)CrossRefGoogle Scholar
  14. 14.
    I. Gulcin, Innov. Food Sci. Emerg. Technol. 11, 210–218 (2010)CrossRefGoogle Scholar
  15. 15.
    I. Gulcin, Arch. Toxicol. 86(3), 345–391 (2012)CrossRefPubMedGoogle Scholar
  16. 16.
    T. Ak, I. Gulcin, Chem. Biol. Interact. 174, 27–37 (2008)CrossRefPubMedGoogle Scholar
  17. 17.
    I. Gulcin, Chem. Biol. Interact. 179(2–3), 71–80 (2009)CrossRefPubMedGoogle Scholar
  18. 18.
    I. Gulcin, R. Elias, A. Gepdiremen, K. Taoubi, E. Köksal, Wood Sci. Technol. 43(3–4), 195–212 (2009)CrossRefGoogle Scholar
  19. 19.
    E. Bursal, I. Gulcin, Food Res. Int. 44(5), 1482–1489 (2011)CrossRefGoogle Scholar
  20. 20.
    I. Gulcin, S. Beydemir, Mini Rev. Med. Chem. 13(3), 408–430 (2013)PubMedGoogle Scholar
  21. 21.
    B. Halliwell, M.A. Murcia, S. Chirico, O.I. Aruoma, Crit. Rev. Food Sci. Nutr. 35, 7–20 (1995)CrossRefPubMedGoogle Scholar
  22. 22.
    I. Gulcin, M. Elmastaş, H.Y. Aboul-Enein, Arab. J. Chem. 5(4), 489–499 (2012)CrossRefGoogle Scholar
  23. 23.
    E. Bursal, E. Köksal, I. Gulcin, G. Bilsel, A.C. Gören, Food Res. Int. 51, 66–74 (2013)CrossRefGoogle Scholar
  24. 24.
    H.C. Ko, J.Y. Lee, M.G. Jang, H. Song, S.J. Kim, Ind. Crops Prod. 122, 506–512 (2018)CrossRefGoogle Scholar
  25. 25.
    S. Çakmakçı, E.F. Topdaş, P. Kalın, H. Han, P. Şekerci, L. Polat Kose, I. Gulcin, Int. J. Food Sci. Technol. 50(2), 472–481 (2015)CrossRefGoogle Scholar
  26. 26.
    Y. Lu, Y. Du, X. Qin, H. Wu, Y. Huang, Y. Cheng, Y. Wei, Ind. Crops Prod. 129, 242–252 (2019)CrossRefGoogle Scholar
  27. 27.
    E. Köksal, I. Gulcin, Turk. J. Agric. For. 32(1), 65–78 (2008)Google Scholar
  28. 28.
    E. Köksal, I. Gulcin, S.B. Öztürk Sarıkaya, E. Bursal, J. Enzyme Inhib. Med. Chem. 24(2), 395–405 (2009)CrossRefPubMedGoogle Scholar
  29. 29.
    I. Gulcin, R. Elias, A. Gepdiremen, A. Chea, F. Topal, J. Enzyme Inhib. Med. Chem. 25(1), 44–53 (2010)CrossRefPubMedGoogle Scholar
  30. 30.
    S.S. Wang, D.M. Wang, Z.H. Liu, Ind. Crops Prod. 67, 227–238 (2015)CrossRefGoogle Scholar
  31. 31.
    I. Gulcin, Z. Huyut, M. Elmastaş, H.Y. Aboul-Enein, Arab. J. Chem. 3, 43–53 (2010)CrossRefGoogle Scholar
  32. 32.
    I. Gulcin, S. Beydemir, F. Topal, N. Gagua, A. Bakuridze, R. Bayram, A. Gepdiremen, J. Enzyme Inhib. Med. Chem. 27(4), 587–594 (2012)CrossRefPubMedGoogle Scholar
  33. 33.
    M.H. Sehitoglu, H. Han, P. Kalin, I. Gulcin, A. Ozkan, H.Y. Aboul-Enein, J. Enzyme Inhib. Med. Chem. 30(2), 264–269 (2015)CrossRefPubMedGoogle Scholar
  34. 34.
    B. Yigit, M. Yiğit, D. Barut Celepci, Y. Gök, A. Aktaş, M. Aygün, P. Taslimi, I. Gulcin, ChemistrySelect 3(27), 7976–7982 (2018)CrossRefGoogle Scholar
  35. 35.
    B. Yigit, R. Kaya, P. Taslimi, Y. Işık, M. Karaman, M. Yiğit, İ. Özdemir, I. Gulcin, J. Mol. Struct. 1179, 709–718 (2019)CrossRefGoogle Scholar
  36. 36.
    A. Bicer, P. Taslimi, G. Yakali, I. Gulcin, M.S. Gültekin, G. Turgut Cin, Bioorg. Chem. 82, 393–404 (2019)CrossRefPubMedGoogle Scholar
  37. 37.
    M. Zengin, H. Genç, P. Taslimi, A. Kestane, E. Güçlü, A. Ögütlü, O. Karabay, I. Gulcin, Bioorg. Chem. 81, 119–126 (2018)CrossRefPubMedGoogle Scholar
  38. 38.
    M. Huseynova, P. Taslimi, A. Medjidov, V. Farzaliyev, M. Aliyeva, G. Gondolova, O. Şahin, B. Yalçın, A. Sujayev, E.B. Orman, A.R. Özkaya, I. Gulcin, Polyhedron 155, 25–33 (2018)CrossRefGoogle Scholar
  39. 39.
    D. Wilkinson, Psychiatry 7, 9–14 (2007)CrossRefGoogle Scholar
  40. 40.
    M. Rezai, Ç. Bayrak, P. Taslimi, I. Gulcin, A. Menzek, Turk. J. Chem. 42, 808–825 (2018)Google Scholar
  41. 41.
    U.M. Kocyigit, Y. Budak, M.B. Gürdere, F. Ertürk, B. Yencilek, P. Taslimi, I. Gulcin, M. Ceylan, Arch. Physiol. Biochem. 124, 61–68 (2018)CrossRefPubMedGoogle Scholar
  42. 42.
    I. Gulcin, P. Taslimi, A. Aygün, N. Sadeghian, E. Bastem, Öİ. Küfrevioğlu, F. Turkan, F. Şen, Int. J. Biol. Macromol. 119, 741–746 (2018)CrossRefPubMedGoogle Scholar
  43. 43.
    P. Taslimi, H.E. Aslan, Y. Demir, N. Öztaşkın, A. Maraş, I. Gulcin, Ş. Beydemir, Ş. Göksu, Int. J. Biol. Macromol. 119, 857–863 (2018)CrossRefPubMedGoogle Scholar
  44. 44.
    Y. Demir, P. Taslimi, M.S. Ozaslan, N. Oztaskın, Y. Çetinkaya, I. Gulcin, S. Beydemir, Arch. Pharm. 351(12), e1800263 (2018)CrossRefGoogle Scholar
  45. 45.
    F. Turkan, A. Çetin, P. Taslimi, I. Gulcin, Arch. Pharm. 351(10), e1800200 (2018)CrossRefGoogle Scholar
  46. 46.
    P.H. Davis, Flora of Turkey and the East Aegean Islands, vol. 1–9(7) (Edinburgh University Press, Edinburgh, 1965–1988), p. 417Google Scholar
  47. 47.
    H. Tohma, I. Gulcin, E. Bursal, A.C. Gören, S.H. Alwasel, E. Köksal, J. Food Meas. 11(2), 556–566 (2017)CrossRefGoogle Scholar
  48. 48.
    P. Kalin, I. Gulcin, A.C. Gören, Rec. Nat. Prod. 9(4), 496–502 (2015)Google Scholar
  49. 49.
    V.L. Singleton, J.A. Rossi, Am. J. Enol. Vitic. 16, 144–158 (1965)Google Scholar
  50. 50.
    I. Gulcin, A.Z. Tel, E. Kirecci, Int. J. Food Prop. 11(2), 450–471 (2008)CrossRefGoogle Scholar
  51. 51.
    I. Gulcin, E. Bursal, H.M. Şehitoğlu, M. Bilsel, A.C. Gören, Food Chem. Toxicol. 48(8–9), 2227–2238 (2010)CrossRefPubMedGoogle Scholar
  52. 52.
    I. Gulcin, F. Topal, R. Çakmakçı, A.C. Gören, M. Bilsel, U. Erdoğan, J. Food Sci. 76(4), C585–C593 (2011)CrossRefPubMedGoogle Scholar
  53. 53.
    M. Oyaizu, Jpn. J. Nutr. 44, 307–315 (1986)CrossRefGoogle Scholar
  54. 54.
    H. Göçer, I. Gulcin, Int. J. Food Sci. Nutr. 62(8), 821–825 (2011)CrossRefPubMedGoogle Scholar
  55. 55.
    I. Gulcin, J. Med. Food 14(9), 975–985 (2011)CrossRefPubMedGoogle Scholar
  56. 56.
    R. Apak, K. Guclu, M. Ozyurek, S.E. Karademir, E. Ercag, Int. J. Food Sci. Nutr. 57, 292–304 (2006)CrossRefPubMedGoogle Scholar
  57. 57.
    E. Köksal, I. Gulcin, Turk. J. Agric. For. 32, 65–78 (2008)Google Scholar
  58. 58.
    O. Talaz, I. Gulcin, S. Göksu, N. Saracoglu, Bioorg. Med. Chem. 17(18), 6583–6589 (2009)CrossRefPubMedGoogle Scholar
  59. 59.
    Y. Çetinkaya, H. Göçer, A. Menzek, I. Gulcin, Arch. Pharm. 345(4), 323–334 (2012)CrossRefGoogle Scholar
  60. 60.
    T.C.P. Dinis, V.M.C. Madeira, L.M. Almeida, Arch. Biochem. Biophys. 315, 161–169 (1994)CrossRefGoogle Scholar
  61. 61.
    Z. Huyut, S. Beydemir, I. Gulcin, Biochem. Res. Int. 2017, 7616791 (2017)CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    F. Ozbey, P. Taslimi, I. Gulcin, A. Maraş, S. Goksu, C.T. Supuran, J. Enzyme Inhib. Med. Chem. 31(S2), 79–85 (2016)CrossRefPubMedGoogle Scholar
  63. 63.
    I.F.F. Benzie, J.J. Strain, Methods Enzymol. 299, 15–27 (1999)CrossRefPubMedGoogle Scholar
  64. 64.
    M.S. Blois, Nature 26, 1199–1200 (1958)CrossRefGoogle Scholar
  65. 65.
    I. Gulcin, Toxicology 217(2–3), 213–220 (2006)CrossRefPubMedGoogle Scholar
  66. 66.
    I. Gulcin, Life Sci. 78(8), 803–811 (2006)CrossRefPubMedGoogle Scholar
  67. 67.
    I. Gulcin, J. Enzyme Inhib. Med. Chem. 23(6), 871–876 (2008)CrossRefPubMedGoogle Scholar
  68. 68.
    H.T. Balaydın, I. Gulcin, A. Menzek, S. Göksu, E. Şahin, J. Enzyme Inhib. Med. Chem. 25(5), 685–695 (2010)CrossRefPubMedGoogle Scholar
  69. 69.
    G.L. Ellman, K.D. Courtney, V. Andres, R.M. Featherston, Biochem. Pharmacol. 7, 88–95 (1961)CrossRefGoogle Scholar
  70. 70.
    A. Akincioglu, H. Akıncıoğlu, I. Gulcin, S. Durdağı, C.T. Supuran, S. Göksu, Bioorg. Med. Chem. 23(13), 3592–3602 (2015)CrossRefPubMedGoogle Scholar
  71. 71.
    N. Oztaskin, Y. Çetinkaya, P. Taslimi, S. Göksu, I. Gulcin, Bioorg. Chem. 60, 49–57 (2015)CrossRefGoogle Scholar
  72. 72.
    Y. Tao, Y. Zhang, Y. Cheng, Y. Wang, Biomed. Chromatogr. 27, 148–155 (2013)CrossRefPubMedGoogle Scholar
  73. 73.
    G. Gondolova, P. Taslimi, A. Medjidov, F. Farzaliyev, A. Sujayev, M. Huseuinova, O. Şahin, B. Yalçın, F. Turkan, I. Gulcin, J. Biochem. Mol. Toxicol. 32(9), e22197 (2018)CrossRefGoogle Scholar
  74. 74.
    Z. Xiao, R. Storms, A. Tsang, Anal. Biochem. 351, 146–148 (2006)CrossRefPubMedGoogle Scholar
  75. 75.
    S.B. Oztürk Sarıkaya, F. Topal, M. Şentürk, I. Gulcin, C.T. Supuran, Bioorg. Med. Chem. Lett. 21(14), 4259–4262 (2011)CrossRefPubMedGoogle Scholar
  76. 76.
    J. Dai, R.J. Mumper, Molecules 15, 7313–7352 (2010)CrossRefPubMedPubMedCentralGoogle Scholar
  77. 77.
    M.J. Del Bano, J. Lorente, J. Castillo, O. Benavente-García, J.A. del Río, A. Ortuno, K.W. Quirin, D.J. Gerard, Environ. Agric. Res. 6, 236–241 (2003)Google Scholar
  78. 78.
    L. Tomsone, Z. Kruma, R. Galoburda, Int. J. Agric. Food Chem. 51, 4247–4253 (2012)Google Scholar
  79. 79.
    V. Georgiev, A. Marchev, M. Nikolova, I. Ivanov, V. Gochev, A. Stoyanova, A. Pavlov, J. Essent. Oil Bear. Plants 16(5), 624–629 (2013)CrossRefGoogle Scholar
  80. 80.
    G. Rafatian, F. Khodagholi, M.M. Farimani, S.B. Abraki, M. Gardaneh, Mol. Cell. Biochem. 371, 9–22 (2012)CrossRefPubMedGoogle Scholar
  81. 81.
    O.S. Adeyemi, O. Atolani, P. Banerjee, G. Arolasafe, R. Preissner, P. Etukudoh, O. Ibraheem, Int. J. Food Prop. 21, 86–98 (2018)CrossRefGoogle Scholar
  82. 82.
    C.A. Rice-Evans, N.J. Miller, G. Paganga, Free Radic. Biol. Med. 20, 933–956 (1996)CrossRefPubMedPubMedCentralGoogle Scholar
  83. 83.
    H. Gocer, A. Akıncıoğlu, N. Öztaşkın, S. Göksu, I. Gulcin, Arch. Pharm. 346(11), 783–792 (2013)CrossRefGoogle Scholar
  84. 84.
    Y. Lu, L.Y. Foo, Phytochemistry 59, 117–140 (2002)CrossRefPubMedGoogle Scholar
  85. 85.
    H. Han, H. Yılmaz, I. Gulcin, Rec. Nat. Prod. 12(4), 397–402 (2018)CrossRefGoogle Scholar
  86. 86.
    N. Oztaskin, P. Taslimi, A. Maraş, S. Göksu, I. Gulcin, Bioorg. Chem. 74, 104–114 (2017)CrossRefPubMedGoogle Scholar
  87. 87.
    M. Kelen, B. Tepe, Bioresour. Technol. 99, 4096–4104 (2008)CrossRefPubMedGoogle Scholar
  88. 88.
    M. Kostic, B. Zlatkovic, B. Miladinovic, S. Zivanovic, T. Mihajilov-Krstev, D. Pavlovic, D. Kitic, J. Food Biochem. 39, 199–208 (2015)CrossRefGoogle Scholar
  89. 89.
    E. Koksal, E. Bursal, I. Gulcin, M. Korkmaz, C. Çağlayan, A.C. Goren, S.H. Alwasel, Int. J. Food Prop. 20(3), 514–525 (2017)CrossRefGoogle Scholar
  90. 90.
    K. Aksu, B. Özgeriş, P. Taslimi, A. Naderi, I. Gulcin, S. Göksu, Arch. Pharm. 349(12), 944–954 (2016)CrossRefGoogle Scholar
  91. 91.
    I. Gulcin, Amino Acids 32, 431–438 (2007)CrossRefPubMedGoogle Scholar
  92. 92.
    S. Okten, M. Ekiz, U.M. Koçyiğit, A. Tutar, İ. Çelik, M. Akkurt, M. Gökalp, P. Taslimi, I. Gulcin, J. Mol. Struct. 1175, 906–915 (2019)CrossRefGoogle Scholar
  93. 93.
    S. Gonçalves, A. Romano, in Phenolic Compounds-Biological Activity, ed. by M. Soto-Hernandez, M. Palma-Tenango, M.R. Garcia-Mateos (InTech, London, 2017), pp. 99–118Google Scholar
  94. 94.
    L. Polat Köse, I. Gulcin, A.C. Gören, J. Namiesnik, A.L. Martinez-Ayala, S. Gorinstein, Ind. Crops Prod. 74, 712–721 (2015)CrossRefGoogle Scholar
  95. 95.
    L.B. Roseiro, A.P. Rauter, M.L.M. Serralheiro, Nutr. Aging 1, 99–111 (2012)Google Scholar
  96. 96.
    N.S.L. Perry, C. Bollen, E.K. Perry, C. Ballard, Pharmacol. Biochem. Behav. 75, 651–659 (2003)CrossRefPubMedGoogle Scholar
  97. 97.
    M.S. Kocak, C. Sarikurkcu, M. Cengiz, S. Kocak, M.C. Uren, B. Tepe, Ind. Crops Prod. 85, 204–212 (2016)CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • İlhami Gülçin
    • 1
    • 2
    Email author
  • Ahmet Zafer Tel
    • 3
  • Ahmet C. Gören
    • 4
    • 5
  • Parham Taslimi
    • 1
  • Saleh H. Alwasel
    • 2
  1. 1.Department of Chemistry, Faculty of SciencesAtatürk UniversityErzurumTurkey
  2. 2.Department of Zoology, College of ScienceKing Saud UniversityRiyadhSaudi Arabia
  3. 3.Department of Agricultural Biotechnology, Faculty of AgricultureIgdir UniversityIgdirTurkey
  4. 4.Department of Analytical Chemistry, Faculty of PharmacyBezmialem Vakif UniversityIstanbulTurkey
  5. 5.Drug Application and Research CenterBezmialem Vakif UniversityIstanbulTurkey

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