Determination of the chemical composition, antioxidant potential of Sambucus ebulus L. (dwarf elder) fruit extracts and investigation of antimicrobial activity on Trichophyton rubrum (Castell.) Sabour and some microorganisms

Yıl 2022, Cilt: 52 Sayı: 2, 148 - 155, 30.08.2022

Serpil Demirci Kayıran , Esra Eroğlu Özkan , Emel Mataracı Kara , Nurdan Yazıcı Bektaş Özden Tarı , Merve Nenni

https://doi.org/10.26650/IstanbulJPharm.2022.929762

Öz

Background and Aims: Sambucus ebulus L. is one of the medicinal plants well known in the traditional medicine of Anatolia since ancient times. The present study was aimed to investigate the antifungal potential of S. ebulus fruit extracts against Trichophyton rubrum (Castell.) Sabour as well as phytochemical composition, antibacterial, and antioxidant activities based on traditional usage.
Methods: Two extracts were prepared from S. ebulus fruits. The phytochemical composition of S. ebulus fruit extracts was identified by LC-MS/MS. The antimicrobial activity was examined by using the broth microdilution method against a panel of microorganisms. In addition to this, S. ebulus extracts were evaluated for their in vitro antifungal activity against three yeast and T. rubrum by disc diffusion method.

Results: The major compounds were determined in dried fruit methanol extract (DFM) as hederagenin (5.38±0.4949 μg/g) and fumaric acid (3.06±0.0275μg/g). The fumaric acid (3.97±0.0357μg/g) was detected as the abundant compound in the fresh fruit juice (FFJ). Acacetin, chrysin, eupatilin, hederagenin, isosakuranetin, myricitrin, and rhamnocitrin were detected in the extracts for the first time. DFM showed moderate activity against E. coli (MIC: 625 mg/L) and Candida tropicalis (MIC: 312.5 mg/L). Both extracts possessed weak activity against Proteus mirabilis and Staphylococcus aureus,which had the MIC values 1250 mg/L. T. rubrum was found resistant to both extracts. The 2,2-diphenyl-1-picrylhydrazyl (DPPH) free radical cleaning method was used to measure the antioxidant capacity of the extracts. DFM and FFJ exhibited strong antioxidant activity against DPPH radicals with IC50 value of 5.941±0.236 μg/mL and 7.893±0.939 μg/mL, respectively.
Conclusion: As a conclusion, although S. ebulus fruits are used to treat nail fungus (onychomycosis) by local folk, our results showed that it could not be useful to use in the antifungal topical formulations. In addition to this, the antibacterial activity result is parallel to the results of studies in this particular so far.

Anahtar Kelimeler

Sambucus ebulus, LC-MS/MS, antifungal activity, Trichophyton rubrum, antioxidant activity

Destekleyen Kurum

Cukurova University BAP

Proje Numarası

(TSA-2019-11424)

Teşekkür

This study was supported by a Cukurova University Fund (TSA-2019-11424). The authors would like to thank Dr. Isil Gazioglu who supported the LC-MS/MS analysis in this study.

Kaynakça

• Ahmadiani, A., Fereidoni, M., Semnanian, S., Kamalinejad, M., & Saremi, S. (1998). Antinociceptive and anti-inflammatory effects of Sambucus ebulus rhizome extract in rats. Journal of Ethnophar- macology, 61(3), 229-235.
• Al-Rifai, A. (2018). Identification and evaluation of in-vitro antioxi- dant phenolic compounds from the Calendula tripterocarpa Rupr. South African Journal of Botany, 116, 238-244.
• Andreicuţ, A.-D., Pârvu, A. E., Moț, A. C., Parvu, M., Fischer-Fodor, E., Feldrihan, V., . . . Irimie, A. (2018). Anti-inflammatory and anti- oxidant effects of Mahonia aquifolium leaves and bark extracts. Farmacia, 66(1), 49.
• Atay, I., Kirmizibekmez, H., Gören, A. C., & Yeşilada, E. (2015). Sec- ondary metabolites from Sambucus ebulus. Turkish Journal of Chemistry, 39(1), 34-41.
• Bakkali, F., Averbeck, S., Averbeck, D., & Idaomar, M. (2008). Biologi- cal effects of essential oils–a review. Food and Chemical Toxicol- ogy, 46(2), 446-475.
• Balea, Ş. S., Pârvu, A. E., Pop, N., Marín, F. Z., & Pârvu, M. (2018). Polyphenolic compounds, antioxidant, and cardioprotective ef- fects of pomace extracts from Fetească Neagră Cultivar. Oxidative Medicine and Cellular Longevity, 2018.
• Blois, M. S. (1958). Antioxidant determinations by the use of a stable free radical. Nature, 181(4617), 1199-1200.
• Braham, F., Carvalho, D., Almeida, C., Zaidi, F., Magalhães, J., Guido, L., & Gonçalves, M. (2020). Online HPLC-DPPH screening method for evaluation of radical scavenging phenols extracted from Moringa oleifera leaves. South African Journal of Botany, 129, 146-154.
• Brand-Williams, W., Cuvelier, M.-E., & Berset, C. (1995). Use of a free radical method to evaluate antioxidant activity. LWT-Food science and Technology, 28(1), 25-30.
• Cvetanović, A. (2020). Sambucus ebulus L., antioxidants and po- tential in disease. In Pathology (pp. 321-333): Elsevier.
• Cvetanovic, A., Djurovic, S., Maskovic, P., Radojkovic, M., Svarc-Ga- jic, J., & Zekovic, Z. (2016). Polyphenolic profile of sambucus ebulus root, leaf and fruit extracts. Zbornik Radova, 21(24), 631-637.
• Cvetanović, A., Zeković, Z., Švarc‐Gajić, J., Razić, S., Damjanović, A., Zengin, G., . . . Moreira, M. (2018). A new source for developing multi‐functional products: biological and chemical perspectives on subcritical water extracts of Sambucus ebulus L. Journal of Chemical Technology & Biotechnology, 93(4), 1097-1104.
• Demirci, S., & Özhatay, N. (2012). An ethnobotanical study in Kahramanmaraş (Turkey); wild plants used for medicinal purpose in Andirin, Kahramanmaraş. Turkish Journal of Pharmaceutical Sci- ences 9(1), 75-92.
• Do, Q. D., Angkawijaya, A. E., Tran-Nguyen, P. L., Huynh, L. H., Soetaredjo, F. E., Ismadji, S., & Ju, Y.-H. (2014). Effect of extraction solvent on total phenol content, total flavonoid content, and antioxidant activity of Limnophila aromatica. Journal of Food and Drug Analysis, 22(3), 296-302.
• Duhard, É. (2014). Les paronychies. La Presse Médicale, 43(11), 1216-1222.
• Ebrahimzadeh, M., Mahmoudi, M., Saiednia, S., Pourmorad, F., & Salimi, E. (2006). Anti-inflammatory and anti-nociceptive proper- ties of fractionated extracts in different parts of Sambucus ebulus. Journal of Mazandaran University of Medical Sciences, 16(54), 35-47.
• Ebrahimzadeh, M., Mahmoudi, M., & Salimi, E. (2006). Antiinflam- matory activity of Sambucus ebulus hexane extracts. Fitoterapia, 77(2), 146-148.
• Ebrahimzadeh, M. A., Ehsanifar, S., & Eslami, B. (2009). Sambucus ebulus elburensis fruits: A good source for antioxidants. Pharma- cognosy Magazine, 5(19), 213.
• Ginovyan, M., & Trchounian, А. (2017). Screening of some plant materials used in Armenian traditional medicine for their antimi- crobial activity. Proceedings of the YSU B: Chemical and Biological Sciences, 51(1), 44-53.
• Glassman, B. P., Bhagwat, D., & Glassman, D. (2004). Method of treat- ing onychomycosis with urea and an antioxidant. In: Google Patents.
• Granato, D., Shahidi, F., Wrolstad, R., Kilmartin, P., Melton, L. D., Hi- dalgo, F. J., . . . Ismail, A. B. (2018). Antioxidant activity, total phe- nolics and flavonoids contents: Should we ban in vitro screening methods? Food Chemistry, 264, 471-475.
• Gupta, A. K., Versteeg, S. G., & Shear, N. H. (2017). Onychomycosis in the 21st century: an update on diagnosis, epidemiology, and treat- ment. Journal of Cutaneous Medicine and Surgery, 21(6), 525-539.
• Gülçin, I., Bursal, E., Şehitoğlu, M. H., Bilsel, M., & Gören, A. C. (2010). Polyphenol contents and antioxidant activity of lyophilized aque- ous extract of propolis from Erzurum, Turkey. Food and Chemical Toxicology, 48(8-9), 2227-2238.
• Han, H., Yilmaz, H., & Gulcin, I. (2018). Antioxidant activity of flax- seed (Linum usitatissimum L.) shell and analysis of its polyphenol contents by LC-MS/MS. Records of Natural Products, 12(4), 397-402.
• Hashemi, Z., Ebrahimzadeh, M. A., & Khalili, M. (2019). Sun pro- tection factor, total phenol, flavonoid contents and antioxidant activity of medicinal plants from Iran. Tropical Journal of Pharma- ceutical Research, 18, 1443-1448.
• Ivanova, D., Tasinov, O., & Kiselova-Kaneva, Y. (2014). Improved lipid profile and increased serum antioxidant capacity in healthy volunteers after Sambucus ebulus L. fruit infusion consumption. International Journal of Food Sciences and Nutrition, 65(6), 740-744.
• Jabbari, M., Daneshfard, B., Emtiazy, M., Khiveh, A., & Hashempur,
• M. H. (2017). Biological effects and clinical applications of dwarf elder (Sambucus ebulus L): A review. Journal of Evidence-Based Complementary & Alternative Medicine, 22(4), 996-1001.
• Kaveh, K., Mohamadyan, M., & Ebrahimzadeh, M. A. (2019). Anti- hypoxic activities of sambucus ebulus leaf and fruit and myrtus communis leaf in mice. Journal of Mazandaran University of Medi- cal Sciences, 29(176), 61-73.
• Kaya, Y., Haji, E. K., Arvas, Y. E., & Aksoy, H. M. (2019). Sambucus ebu- lus L.: Past, present and future. Paper presented at the AIP Confer- ence Proceedings.
• Kedare, S. B., & Singh, R. (2011). Genesis and development of DPPH method of antioxidant assay. Journal of Food Science and Technology, 48(4), 412-422.
• Kültür, Ş. (2007). Medicinal plants used in Kırklareli province (Tur- key). Journal of Ethnopharmacology, 111(2), 341-364.
• Lipner, S. R., & Scher, R. K. (2019). Onychomycosis: Treatment and prevention of recurrence. Journal of the American Academy of Der- matology, 80(4), 853-867.
• Meriç, Z. İ., Bitiş, L., Birteksöz-Tan, S., Turan, S. Ö., & Akbuga, J. (2014). Antioxidant, antimicrobial and anticarcinogenic activities of Sam- bucus ebulus L. flowers, fruits and leaves. Marmara Pharmaceutical Journal, 18(1), 22-25. doi:10.12991/mpj.201414122
• Meza, A., Rojas, P., Cely-Veloza, W., Guerrero-Perilla, C., & Coy- Barrera, E. (2020). Variation of isoflavone content and DPPH• scavenging capacity of phytohormone-treated seedlings after in vitro germination of cape broom (Genista monspessulana). South African Journal of Botany, 130, 64-74.
• Mikulic‐Petkovsek, M., Ivancic, A., Todorovic, B., Veberic, R., & Stam- par, F. (2015). Fruit phenolic composition of different elderberry species and hybrids. Journal of Food Science, 80(10), C2180-C2190.
• Morais, S., Lima, K., Siqueira, S., Cavalcanti, E., Souza, M., Menezes, J., & Trevisan, M. (2013). Correlação entre as atividades antiradi- cal, antiacetilcolinesterase e teor de fenóis totais de extratos de plantas medicinais de farmácias vivas. Revista Brasileira de Plantas Medicinais, 15, 575-582.
• Nogueira, A. C., Morais, S. M. d., Souza, E. B. d., Albuquerque, M. R. J. R., Santos, H. S. d., Cavalcante, C. S. d. P., . . . Fontenelle, R. O. d. S. (2020). Antifungal and antioxidant activities of Vernonia chalybaea Mart. ex DC. essential oil and their major constituent β-caryophyllene. Brazilian Archives of Biology and Technology, 63.
• Pârvu, M., Moţ, C. A., Pârvu, A. E., Mircea, C., Stoeber, L., Roşca- Casian, O., & Ţigu, A. B. (2019). Allium sativum extract chemical composition, antioxidant activity and antifungal effect against Meyerozyma guilliermondii and Rhodotorula mucilaginosa caus- ing onychomycosis. Molecules, 24(21), 3958.
• Rodino, S., Butu, A., Petrache, P., Butu, M., Dinu-Pirvu, C.-E., & Cor- nea, C. P. (2015). Evaluation of the antimicrobial and antioxidant activity of Sambucus ebulus extract. Farmacia, 63(5), 751-754.
• Salehzadeh, A., Asadpour, L., Naeemi, A. S., & Houshmand, E. (2014). Antimicrobial activity of methanolic extracts of Sambu- cus ebulus and Urtica dioica against clinical isolates of methicil- lin resistant Staphylococcus aureus. African Journal of Traditional, Complementary and Alternative Medicines, 11(5), 38-40.
• Scopel, M., Nunes, E. C. M., Silva, M. V., Vendruscolo, G. S., Henriques, A. T., & Mentz, L. A. (2007). Caracterização farmacobotânica das es- pécies de Sambucus (Caprifoliaceae) utilizadas como medicinais no Brasil: Parte I. Sambucus nigra L. Revista brasileira de farmacognosia. São Paulo, SP. Vol. 17, n. 2 (Abr./Jun. 2007), p. 249-261.
• Senica, M., Stampar, F., & Mikulic-Petkovsek, M. (2019). Harmful (cyanogenic glycoside) and beneficial (phenolic) compounds in different Sambucus species. Journal of Berry Research, 9(3), 395-409.
• Shi, D., Lu, G., Mei, H., De Hoog, G. S., Zheng, H., Liang, G., . . . Liu, W. (2016). Onychomycosis due to Chaetomium globosum with yel- lowish black discoloration and periungual inflammation. Medical Mycology Case Reports, 13, 12-16.
• Shokrzadeh, M., & Saravi, S. S. (2010). The chemistry, pharmacol- ogy and clinical properties of Sambucus ebulus: A review. Journal of Medicinal Plants Research, 4(2), 95-103.
• Sinikumpu, S.-P., Huilaja, L., Auvinen, J., Jokelainen, J., Puukka, K., Ruokonen, A., . . . Tasanen, K. (2018). The association between low grade systemic inflammation and skin diseases: a cross-sectional survey in the Northern Finland birth cohort 1966. Acta Dermato- Venereologica, 98(1-2), 65-69.
• Süntar, I. P., Akkol, E. K., Yalçın, F. N., Koca, U., Keleş, H., & Yesilada, E. (2010). Wound healing potential of Sambucus ebulus L. leaves
• and isolation of an active component, quercetin 3-O-glucoside. Journal of Ethnopharmacology, 129(1), 106-114.
• Topuzović, M. D., Stanković, M. S., Jakovljević, D. Z., & Bojović, B. M. (2016). Plant part variability of Sambucus ebulus L. secondary metabolites content and antioxidant activity. Agro Food Ind Hi Technol, 27(2), 60-64.
• Tuzlacı, E., & Tolon, E. (2000). Turkish folk medicinal plants, part III: Şile (Istanbul). Fitoterapia, 71(6), 673-685.
• Vankova, D. V., Todorova, M. N., Kisselova-Kaneva, Y. D., & Galunska, B. T. (2019). Development of new and robust LC-MS method for simultaneous quantification of polyphenols from Sambucus ebu- lus fruits. Journal of Liquid Chromatography & Related Technologies, 42(13-14), 408-416.
• Yesilada, E. (1997). Evaluation of the anti-inflammatory activity of the Turkish medicinal plant Sambucus ebulus. Chemistry of Natural Compounds, 33(5), 539-540.
• Yesilada, E., Gürbüz, İ., & Toker, G. (2014). Anti-ulcerogenic activ- ity and isolation of the active principles from Sambucus ebulus L. leaves. Journal of Ethnopharmacology, 153(2), 478-483.
• Zahmanov, G., Alipieva, K., Denev, P., Todorov, D., Hinkov, A., Shish- kov, S., . . . Georgiev, M. I. (2015).