GC-MS Analysis and Biological Activities of Algerian Salvia microphylla Essential Oils

  • Hafsa Chouit University Blida 1
  • Ouassila Touafek University Blida 1
  • Moussa Brada Djilali Bounaama University of Khemis-Miliana
  • Chawki Benssouici Biotechnology Research Center (CRBT)
  • Marie-Laure Fauconnier University of Liège
  • Mohamed El Hattab University Blida 1
Keywords: Salvia microphylla, GC-MS analysis, antioxidant, anticholinesterase, antimicrobial

Abstract

Abstract. Salvia microphylla is a known species due to its broad uses in traditional medicine against memory loss and rheumatism. The knowledge regarding the chemical composition and biological activities of the species collected in Algeria, no studies have been reported in the literature. Therefore, the present work focuses on the characterization of the chemical composition of the essential oils (EOs) and the determination of the antioxidant, anticholinesterase, α-glucosidase, and antimicrobial activities of Salvia microphylla. The EOs were obtained by hydrodistillation from the aerial parts, leaves and stems and submitted to chemical analysis by GC and GC/MS. The β-Caryophyllene was identified as the main constituent in the aerial parts and leaves essential oils with 16.75 ± 0.02 % and 17.86 ± 0.07 %, respectively. Likewise, the α-Eudesmol was the predominant component in the stems oil with (21.47 ± 0.20 %). The antioxidant activity of EOs was estimated through using four comparative methods: DPPH, ABTS•+, Reducing power and CUPRAC assays. The Stems oil was the most active one in CUPRAC assay, with an IC50 value with 7.72 ± 0.43 µg/mL. The enzyme inhibitory activity of the essential oils was realized against key enzymes involved in type 2 diabetes (α-glucosidase) using 4-Nitrophenyl-α-d-glucopyranoside as substrate and in neurodegenerative (AChE and BChE) diseases. The highest anticholinesterase activity against acetylcholinesterase was observed in the EO of aerial parts essential  (IC50: 23.65 ± 0.73 µg/mL). The EO isolated from stems (IC50: 37.07 ± 1.44 µg/mL) exhibited a butyrylcholinesterase activity very close to that of analytical standard galantamine (IC50: 34.75 ± 1.99 µg/mL). Furthermore, all EOs displayed high inhibitory activity against α-glucosidase, better to that of the standard acarbose. The EOs of Salvia microphylla display potential properties against type 2 diabetes. A broth microdilution method was used to evaluate the antimicrobial activity of Salvia microphylla EOs, against eleven microbial strains and two yeast. The EOs showed better antibacterial activity against Gram-positive and Gram-negative bacteria except for Pseudomonas aeruginosa, with the stems essential oil being more efficient. Moreover, significant antifungal activity was observed against Candida albicans.

 

Resumen. Salvia microphylla es una specie conocida debido a su amplio uso en medicina tradicional, contra la pérdida de memoria y el reumatismo. En el caso de la especie de planta recolectada en Algeria, no hay datos publicados sobre su composición química y sus actividades biológicas. Por ello, el presente trabajo ha sido enfocado en la caracterización de la composición química de aceites esenciales (EOs) de Salvia microphylla y en la determinación de sus actividades antioxidante, anticolinesterasa, α-glucosidasa y antimicrobiano. Los EOs fueron obtenidos mediante hidrodestilación de las partes aéreas, ojas y tallos, y fueron sometidos al análisis por cromatografía de gases con detección por ionización en flama y por espectrometría de masas. Se identificó a β-cariofileno como el componente principal de los aceites de las partes aéreas y de tallos con concentraciones de 16.75 ± 0.02 % y 17.86 ± 0.07 %, respectivamente. Por su parte, el α-Eudesmol fue encontrado como componente predominante en aceite de tallos (21.47 ± 0.20 %). La actividad antioxidante de los EOs fue estimada en base a cuatro métodos compartivos: DPPH, ABTS•+, poder reductor y ensayo CUPRAC. El aceite de tallos resultó ser el más activo en ensayo CUPRAC, con el valor IC50 de 7.72 ± 0.43 µg/mL. La actividad inhibitora de enzimas de los EOs fue evaluada contra principales enzimas involucrados en diabetes tipo 2 (α-glucosidasa), utilizando 4-Nitrofenil-α-d-glucopiranosida como sustrato, y en enfermedades neurodergenerativas (AChE y BChE). La mayor actividad anticolinesterasa y acetilcolinesterasa fue observada en el EO de partes aéreas (IC50: 23.65 ± 0.73 µg/mL). El EO islado de tallos (IC50: 37.07 ± 1.44 µg/mL) presentó actividad de butirilcolinestarasa muy similar a la del estándar analítico, galantamina (IC50: 34.75 ± 1.99 µg/mL). Aunado a ello, todos EOs presentaron una alta actividad inhibitora contra α-glucosidasa, que era mejor comparando con la del estándar de acarbosa. Los EOs de Salvia microphylla presentan potenciales propiedades contra diabetes tipo 2. Para evaluar la actividad antimicrobiana de los EOs de Salvia microphylla, se utilizó el método de microdulución en caldo, contra once sepas microbianas y dos de levadura. La mejor actividad se observó contra bacterias Gram-positivas y Gram-negativas, excepto Pseudomonas aeruginosa, los cuales presentaron alta resistencia. Los EOs presentaron también importante actividad antifungica contra Candida albicans.

Author Biographies

Hafsa Chouit, University Blida 1

Laboratory of Natural Products Chemistry and Biomolecules.

Ouassila Touafek, University Blida 1

Laboratory of Natural Products Chemistry and Biomolecules.

Moussa Brada, Djilali Bounaama University of Khemis-Miliana

Valuation of Natural Substances Laboratory.

Marie-Laure Fauconnier, University of Liège

Laboratory of Chemistry of Natural Molecules, Gembloux Agro-Bio Tech.

Mohamed El Hattab, University Blida 1

Laboratory of Natural Products Chemistry and Biomolecules.

References

Bakkali, F.; Averbeck, S.; Averbeck, D.; Idaomar M. Food Chem. Toxicol. 2008, 46, 446-475. DOI: https://doi.org/10.1016/j.fct.2007.09.106

Hedge, I.C. Advances in Labiatae science. 1992, 7-17.

Kabouche, A.; Kabouche, Z. Stud. Nat. Prod. Chem. 2008, 753-833. DOI: https://doi.org/10.1016/S1572-5995(08)80017-8

Medjahed, F.; Merouane, A.; Saadi, A.; Bader, A.; Cioni, P.L.; Flamini, G. Chilean J. Agric. Res. 2016, 76, 195-200. DOI : http://dx.doi.org/10.4067/S0718-58392016000200009

Beladjila, K.A.; Berrehal, D.; Al-Aboudi, A.; Semra, Z.; Al-Jaber, H.; Bachari, K.; Kabouche, Z. Chem. Nat. Compd. 2018, 54, 581-583. DOI : https://doi.org/10.1007/s10600-018-2414-z

Şenol, F.S.; Orhan, I.; Celep, F.; Kahraman, A.; Doğan, M.; Yilmaz, G.; Şener, B. Food Chem. 2010, 120, 34-43. DOI: https://doi.org/10.1016/j.foodchem.2009.09.066

Kamatou, G.P.P.; Makunga, N.P.; Ramogola, W.P.N.; Viljoen, A.M. J. Ethnopharmacol. 2008a, 119, 664-672. DOI: https://doi.org/10.1016/j.jep.2008.06.030

Kamatou, G.P.; Van Zyl, R.; Davids, H.; Van Heerden, F.; Lourens, A.; Viljoen, A.M. S. Afr. J. Bot. 2008b, 74, 238-243. DOI: https://doi.org/10.1016/j.sajb.2007.08.001

Kivrak, İ.; Duru, M.E.; Öztürk, M.; Mercan, N.; Harmandar, M.; Topçu, G. Food chem. 2009, 116, 470-479. DOI: https://doi.org/10.1016/j.foodchem.2009.02.069

Tel, G.; Öztürk, M.; Duru, M.E.; Harmandar, M.; Topçu, G. Food Chem. Toxicol. 2010, 48, 3189-3193. DOI : https://doi.org/10.1016/j.fct.2010.08.020

Al-Jaber, H.I.; Al-Qudah, M.A.; Barhoumi, L.M.; Abaza, I.F.; Afifi, F.U. Nat. Prod. Res. 2012, 26, 1179-1187. DOI: https://doi.org/10.1080/14786419.2010.543901

Coisin, M.; Burzo, I.; Stefan, M.; Rosenhech, E.; Zamfirache, M.M. An. Stiint. Univ. Al. I. Cuza Iasi, Sect. II a. Biol. veget. 2012, 58, 51-58.

Marchev, A.; Ivanov, I.; Denev, P.; Nikolova, M.; Gochev, V.; Stoyanova, A.; Pavlov, A.; Georgiev, V. Journal of BioScience & Biotechnology. 2015, 4.

Russo, A.; Formisano, C.; Rigano, D.; Cardile, V.; Arnold, N.A.; Senatore, F. Ind. Crops Prod. 2016, 83, 492-499. DOI: https://doi.org/10.1016/j.indcrop.2015.12.080

Temel, H.E.; Demirci, B.; Demirci, F.; Celep, F.; Kahraman, A.; Doğan, M.; Hüsnü Can Başer, K. J. Essent. Oil Res. 2016, 28, 322-331. DOI :https://doi.org/10.1080/10412905.2016.1159257

El Euch, S.K.; Hassine, D.; Cazaux, S.; Bouzouita, N.; Bouajila, J. S. Afr. J. Bot. 2019, 120, 253-260. DOI: https://doi.org/10.1016/j.sajb.2018.07.010

Süzgeç-Selçuk, S.; Özek, T.; Özek, G.; Yur, S.; Göger, F.; Gürdal, M.B.; Toplan, G.G.; Meriçli, A.H.; Başer, K.H.C. Rec. Nat. Prod. 2021, 15, 10-24. DOI: http://doi.org/10.25135/rnp.185.20.03.1579

Crespo, M.E.; Jimenez, J.; Navarro, C.; Zarzuelo, A. Planta Med. 1986, 52, 367-369. DOI: 10.1055/s-2007-969187

Perry, N.S.L.; Houghton, P.J.; Sampson, J.; Theobald, A.E.; Hart, S.; Lis-Balchin, M.; Hoult, J.R.S.; Evans, P.; Jenner, P.; Milligan, S.; Perry, E.K. J. Pharm. Pharmacol. 2001, 53, 1347-1356. DOI: https://doi.org/10.1211/0022357011777846

Jirovetz, L.; Buchbauer, G.; Denkova, Z.; Slavchev, A.; Stoyanova, A.; Schmidt, E. Nutrition-Vienna. 2006, 30, 152.

Nikolić, M.; Jovanović, K.K.; Marković, T.; Marković, D.; Gligorijević, N.; Radulović, S.; Soković, M. Ind. Crops Prod. 2014, 61, 225-232. DOI: https://doi.org/10.1016/j.indcrop.2014.07.011

Adrar, N.; Oukil, N.; Bedjou, F. Ind. Crops Prod. 2016, 88, 112-119. DOI: https://doi.org/10.1016/j.indcrop.2015.12.007

Bahadori, M.B.; Dinparast, L.; Zengin, G.; Sarikurkcu, C.; Bahadori, S.; Asghari, B.; Movahhedin, N. Int. J. Food Prop. 2017a, 20, 1761-1772. DOI: https://doi.org/10.1080/10942912.2016.1218893

Bahadori, M.B.; Salehi, P.; Sonboli, A. Int. J. Food Prop. 2017b, 20, 2974-2981. DOI: https://doi.org/10.1080/10942912.2016.1263862

Valdés, B.; Martín, M.; Díaz, Z. Bot. Macaron. 1995, 21, 107-120.

Jenks, A.A.; Kim, S.-C. J. Ethnopharmacol. 2013, 146, 214-224. DOI: https://doi.org/10.1016/j.jep.2012.12.035

Béjar, E.; Bussmann, R.; Roa, C.; Sharon, D. Latin Herbal Press, San Diego. 2001.

Lima, R.K.; dasGraças Cardoso, M.; Andrade, M.A.; Guimarães, P.L.; Batista, L.R.; Nelson, D.L. J. Am. Oil Chem. Soc. 2012, 89, 523-528. DOI: https://doi.org/10.1007/s11746-011-1938-1

Romo-Asunción, D.; Ávila-Calderón, M.A.; Ramos-López, M.A.; Barranco-Florido, J.E.; Rodríguez-Navarro, S.; Romero-Gomez, S.; Aldeco-Pérez, E.J.; Pacheco-Aguilar, J.R.; Rico-Rodríguez, M.A. Fla. Entomol. 2016, 345-351. DOI: https://www.jstor.org/stable/24891070

Aydoğmuş, Z.; Yeşİlyurt, V.; Topcu, G. Nat. Prod. Res. 2006, 20, 775-781. DOI: https://doi.org/10.1080/14786410500462843

Esquivel, B.; Cardenas, J.; Rodriguez-Hahn, L.; Ramamoorthy, T. J. Nat. Prod. 1987, 50, 738-740. DOI: https://doi.org/10.1021/np50052a029

Esquivel, B.; del Socorro Martínez, N.; Cárdenas, J.; Ramamoorthy, T.; Rodríguez-Hahn, L. Planta Med. 1989, 55, 62-63. DOI: 10.1055/s-2006-961827

Bautista, E.; Toscano, R.A.; Ortega, A. Org. Lett. 2013, 15, 3210-3213. DOI: https://doi.org/10.1021/ol401022c

Bautista, E.; Toscano, R.n.A.; Ortega, A. J. Nat. Prod. 2014, 77, 1088-1092. DOI: https://doi.org/10.1021/np4009893

Chialva, F.; Monguzzi, F.; Manitto, P. J. Essent. Oil Res. 1992, 4, 447-455. DOI: https://doi.org/10.1080/10412905.1992.9698108

Koutsaviti, A.; Antonopoulou, V.; Vlassi, A.; Antonatos, S.; Michaelakis, A.; Papachristos, D.P.; Tzakou, O. Journal of pest science. 2018, 91, 873-886. DOI: https://doi.org/10.1007/s10340-017-0934-0

Marchioni, I.; Najar, B.; Ruffoni, B.; Copetta, A.; Pistelli, L.; Pistelli, L. Plants. 2020, 9, 691. DOI: https://doi.org/10.3390/plants9060691

National Committee for Clinical Laboratory Standards (NCCLS), Wayne, PA. New York. M2-A6. 1997.

Clinical and laboratory standards institute. Quality Control Minimal Inhibitory Concentration (MIC) Limits for Broth Microdilution and MIC Interpretive Breakpoints. Supplement M27-S2. 2006.

Joulain, D.; König, W. Verlag: EB-Verlag, Hamburg, Germany. 1998.

Adams, R.P. Quadruple mass spectroscopy. Allured Publishing Corporation, Carol. Stream, IL, USA, 2001, 456.

Van Den Dool, H.; Kratz, P. D. A. J. Chromatogr. A. 1963, 11, 463-471.

Goldschmidt, S.; Renn, K. Ber. Dtsch. Chem. Ges. A. B. 1922, 55, 628-643. DOI: https://doi.org/10.1002/cber.19220550308

Osman, A.M. Biochem. Biophys. Res. Commun. 2011, 412, 473-478. DOI: https://doi.org/10.1016/j.bbrc.2011.07.123

Passari, A. K.; Leo, V. V.; Singh, G.; Samanta, L.; Ram, H.; Siddaiah, C. N.; Hashem, A.; Al-Arjani, A.-B. F.; Alqarawi, A. A.; Fathi Abd_Allah, E. Int. J. Mol. Sci. 2020, 21, 7364. DOI: https://doi.org/10.3390/ijms21197364

Ražná, K.; Sawinska, Z.; Ivanišová, E.; Vukovic, N.; Terentjeva, M.; Stričík, M.; Kowalczewski, P. Ł.; Hlavačková, L.; Rovná, K.; Žiarovská, J. Int. J. Mol. Sci. 2020, 21, 3087. DOI: https://doi.org/10.3390/ijms21093087

Mishra, K.; Ojha, H.; Chaudhury, N.K. Food Chem. 2012, 130, 1036-1043. DOI: https://doi.org/10.1016/j.foodchem.2011.07.127

Re, R.; Pellegrini, N.; Proteggente, A.; Pannala, A.; Yang, M.; Rice-Evans, C. Free Radicals Biol. Med. 1999, 26, 1231-1237. DOI: https://doi.org/10.1016/S0891-5849(98)00315-3

Apak, R.; Güçlü, K.; Özyürek, M.; Karademir, S.E. J. Agric. Food Chem. 2004, 52, 7970-7981. DOI: https://doi.org/10.1021/jf048741x

Oyaizu, M. Jpn. J. Nutr. Diet. 1986, 44, 307-315. DOI : https://doi.org/10.5264/eiyogakuzashi.44.307

Ellman, G.L.; Courtney, K.D.; Andres Jr, V.; Featherstone, R.M. Biochem. Pharmacol. 1961, 7, 88-95. DOI: https://doi.org/10.1016/0006-2952(61)90145-9

Lordan, S.; Smyth, T.J.; Soler-Vila, A.; Stanton, C.; Ross, R.P. Food Chem. 2013, 141, 2170-2176. DOI: https://doi.org/10.1016/j.foodchem.2013.04.123

Amrani, A.; Mecheri, A.; Bensouici, C.; Boubekri, N.; Benaissa, O.; Zama, D.; Benayache, F.; Benayache, S. Biocatal. Agric. Biotechnol. 2019, 20, 101209. DOI: https://doi.org/10.1016/j.bcab.2019.101209

Approved Standard-National Committee for Clinical Laboratory Standards Wayne, PA. 2008, 28, M27-A3.

Approved Standard-Tenth Edition; Document M07-A10; Clinical and Laboratory Standards Institute: Wayne, PA. 2015.

Cutillas, A.B.; Carrasco, A.; Martinez-Gutierrez, R.; Tomas, V.; Tudela, J. Mol. 2017, 22, 1382. DOI: https://doi.org/10.3390/molecules22081382

Balouiri, M.; Sadiki, M.; Ibnsouda, S.K. J. Pharm. Anal. 2016, 6, 71-79. DOI: https://doi.org/10.1016/j.jpha.2015.11.005

Martínez-Francés, V.; Hahn, E.; Ríos, S.; Rivera, D.; Reich, E.; Vila, R.; Cañigueral, S. Front. Pharmacol. 2017, 8, 467. DOI: https://doi.org/10.3389/fphar.2017.00467

Mata, A.; Proença, C.; Ferreira, A.; Serralheiro, M.; Nogueira, J.; Araújo, M. Food Chem. 2007, 103, 778-786. DOI: https://doi.org/10.1016/j.foodchem.2006.09.017

Ruberto, G.; Baratta, M.T. Food Chem. 2000, 69,167-174. DOI: https://doi.org/10.1016/S0308-8146(99)00247-2

Loizzo, M.R.; Tundis, R.; Conforti, F.; Menichini, F.; Bonesi, M.; Nadjafi, F.; Frega, N.G.; Menichini, F. Nutr. Res. 2010, 30, 823-830. DOI: https://doi.org/10.1016/j.nutres.2010.09.016

Fu, Z.; Wang, H.; Hu, X.; Sun, Z.; Han, C. J. Appl. Pharm. Sci. 2013, 3, 122-127. DOI: 10.7324/JAPS.2013.3723

Vladimir-Knezevic, S.; Blazekovic, B.; Kindl, M.; Vladic, J.; Lower-Nedza, A.D.; Brantner, A.H. Mol. 2014, 19, 767-782. DOI: https://doi.org/10.3390/molecules19010767

Perry, N.S.; Houghton, P.J.; Jenner, P.; Keith, A.; Perry, E.K. Phytomedicine. 2002, 9, 48-51. DOI: https://doi.org/10.1078/0944-7113-00082

Savelev, S.U.; Okello, E.J.; Perry, E.K. Phytother. Res. 2004, 18, 315-324. DOI: https://doi.org/10.1002/ptr.1451

Duru, M.E.; Tel, G.; Öztürk, M.; Harmandar, M. Rec. Nat. Prod. 2012, 6, 175-179.

Salinas, M.; Bec, N.; Calva, J.; Ramírez, J.; Andrade, J.M.; Larroque, C.,; Vidari, G.; Armijos, C. Rec. Nat. Prod. 2020, 14, 276-285. DOI: http://doi.org/10.25135/rnp.164.19.07.1342

Savelev, S.; Okello, E.; Perry, N.S.; Wilkins, R.M.; Perry, E.K. Pharmacol., Biochem. Behav. 2003, 75, 661-668. DOI: https://doi.org/10.1016/S0091-3057(03)00125-4

Loizzo, M.R.; Menichini, F.; Tundis, R.; Bonesi, M.; Conforti, F.; Nadjafi, F.; Statti, G.A.; Frega, N.G.; Menichini, F. J. Oleo Sci. 2009, 58, 443-446. DOI: https://doi.org/10.5650/jos.58.443

Bahadori, M.B.; Valizadeh, H.; Asghari, B.; Dinparast, L.; MoridiFarimani, M.; Bahadori, S. J. Funct. Foods. 2015, 18, 727-736. DOI:https://doi.org/10.1016/j.jff.2015.09.011

Burt, S. Int. J. Food Microbiol. 2004, 94, 223-253. DOI: https://doi.org/10.1016/j.ijfoodmicro.2004.03.022

Mourey, A.; Canillac, N. Food Control. 2002, 13, 289-292. DOI: https://doi.org/10.1016/S0956-7135(02)00026-9

Koroch, A. R.; Juliani, H. R.; Zygadlo, J. A. Flavours Fragrances. 2007, 87-115. DOI: https://doi.org/10.1007/978-3-540-49339-6_5

Traoré, Y.; Ouattara, K.; Yéo, D.; Doumbia, I.; Coulibaly, A. J. Appl. Biosci. 2012, 58, 4234-4242.

Mastelic, J.; Politeo, O.; Jerkovic, I.; Radosevic, N. Chem. Nat. Compd. 2005, 41, 35-40. DOI: https://doi.org/10.1007/s10600-005-0069-z

Published
09-23-2021
Section
Regular Articles