Composition and biological activity of Brazilian rose pepper (Schinus terebinthifolius Raddi) leaves

https://doi.org/10.1016/j.indcrop.2015.11.077Get rights and content

Highlights

  • Antimicrobial and antioxidant activities of S. terebinthifolius were evaluated.

  • Phenolic acids and flavonoids were found in the extracts by LC–ESI–MS/MS.

  • Δ3-Carene (68.78%) was the majority compound in the essential oil.

  • Ethanolic extracts exhibited strong antioxidant and antimicrobial activity.

  • The results justify the folk medicine use in urinary tract infection.

Abstract

The leaves of Schinus terebinthifolius Raddi (Anacardiaceae), the Brazilian pepper tree, are widely used in folk medicine for treating human diseases caused by microorganisms. The aim of the present study was to investigate the antioxidant and antimicrobial activity and the chemical composition of S. terebinthifolius leaf extract and essential oil. Essential oil from fresh leaves of S. terebinthifolius was obtained in a Clevenger-type apparatus. Ethanol leaves extracts were prepared by maceration and ultrasound assisted extraction. Antimicrobial activity was tested at concentrations up to 1000 μg/ml by the microdilution test after 24 h and antioxidant activity was investigated using the DPPH (2,2-diphenyl-1-picrylhydrazyl) radical-scavenging assay. Phenolic compounds were determined by the Folin–Cioucalteu method and flavonoids by the aluminum chloride technique. The chemical composition of the essential oil and the extracts were characterized by GC/MS and LC–MS/MS, respectively. Ultrasound assisted extraction exhibited higher yield (182.25 ± 3.00 mg/g) and flavonoid content (243.09 ± 8.83 mg/g), while the extraction method of maceration showed higher content of total phenolic compounds (221.63 ± 2.58 mg/g) and exhibited strong antioxidant activity (IC50 15.43 μg/ml). All extracts showed strong antimicrobial activity against Staphylococcus aureus and Escherichia coli. Thirty-two constituents were identified in the oil (97.90% of the total), with δ-3-carene (68.78%), E-caryophyllene (8.22%), myrcene (6.78%) and α-pinene (4.05%) as the main compounds. Mass spectrometry analyzes revealed that ferulic and caffeic acids, and quercetin were the major components in the extracts. In summary, these findings demonstrate the potential antioxidant and antimicrobial activity of extracts that may help to explain the popular use for urinary tract infection of S. terebinthifolius.

Introduction

Urinary tract infection (UTI) is considering one of the most common human infections, affecting all ages especially in women (Kucheria et al., 2005). UTI remains a major public health problem in terms of morbidity and financial cost (Al-Badr and Al-Shaikh, 2013). The main etiologic agents in UTI are Escherichia coli, Staphylococcus aureus, Candida albicans, Enterococcus faecalis, Pseudomonas aeruginosa, Klebsiella pneumonia, and Proteus mirabilis. E. coli is the main microorganism that causes UTIs in most patients and recurrent UTIs are mainly attributed by reinfection of the same pathogen (Svanborg and Godaly, 1997, Al-Badr and Al-Shaikh, 2013). The initial treatment of UTIs is based on antimicrobial therapy, however due to the continuous and indiscriminate use of antibiotics various pathogenic bacteria have developed resistance to many of the currently available antibiotics (Gupta et al., 2001).

Antimicrobials derived from the plants have been receiving increasing attention and there is a continuous need to discover new antimicrobials with diverse chemical structures and novel mechanism of action for the treatment of new and reemerging infectious diseases including UTI (Sharma et al., 2013). Therefore, medicinal plants that have been used for centuries in folk medicine are a promising alternative for searching new prototypes lead compounds to develop more effective and less toxic medicines (Sharma et al., 2013). The presence of the secondary metabolites, especially phenolic compounds, flavonoids and terpenoids have been described in the literature to possess potential antioxidant and antimicrobial activity (Ravikumar et al., 2010).

Schinus terebinthifolius Raddi, commonly known as aroeira in Brazil, belongs to the Anacardiaceae family and is largely distributed in Brazilian territory, mainly in the Atlantic Forest (Wheeler et al., 2001). S. terebinthifolius can also be found in tropical and semitropical regions of the United States and Africa (Campelo and Marsaioli, 1974). The fruits, commonly known as rose pepper, have great interest in the food industries because its flavor and aroma. In the folk medicine, S. terebinthifolius has been used for treatment of respiratory problems, wounds, rheumatism, as anti-inflammatory and hemostatic agent, for treatment of urinary and respiratory infections, as well as aid for prevention of cancer through its antioxidant properties (Melo-Junior et al., 2002, El-Massry et al., 2009).

Previous phytochemical studies of this species have resulted in the isolation of many monoterpenes, sesquiterpenes, triterpenes, flavonoids and proteins (El-Massry et al., 2009, Matsuo et al., 2011). Leaf extract and essential oil from fruits of S. terebinthifolius were reported to possess larvicidal effect against Stegomia aegypti larvae (Silva et al., 2010) and Aedes aegypti larvae (Procópio et al., 2015). Alpha-pinene isolated from leaves exhibited great potential to induce apoptosis on melanoma cancer cells (Matsuo et al., 2011). The aromatic compounds, gallic acid and methyl gallate, as major compounds in the acetate fraction, exhibited important anti-allergic properties (Cavalher-Machado et al., 2008). Lectin isolated from the leaves showed strong antimicrobial activity with bactericide and fungicide properties (Gomes et al., 2013).

Combining popular knowledge by using aroeira for the UTI treatment with the increasing resistance of microorganism, this study investigated the chemical composition as well as antioxidant and antimicrobial activity of S. terebinthifolius leaves against the main bacteria involved in urinary tract infection.

Section snippets

Materials

The radical 2,2-diphenyl-1-picryl-hydrazyl (DPPH), butylated hydroxytoluene (BHT), ferulic acid, caffeic acid, chlorogenic acid, gallic acid, rosmarinic acid, apigenin, quercetin, Folin–Ciocalteau reagent, sodium carbonate, and triphenyl tetrazolium chloride (TTC) were purchased from Sigma Chemical Co., MO, USA. All solvents and reagents including acetone, ethanol, methanol, aluminum chloride, acetic acid, methenamine, hydrochloric acid, ethyl acetate, magnesium sulfate, and dimethylsulfoxide

Results and discussion

Table 1 shows the extraction yield, total phenolic and total flavonoid content of S. terebinthifolius leaf ethanolic extract and essential oil quantified by Folin–Ciocalteau assay and using a colorimetric assay with aluminum chloride, respectively. Ultrasound assisted extraction technique exhibited the highest yield of crude extract followed by the maceration method and finally the hydro-distillation technique (p < 0.05) (Table 1). The obtained higher yield, using ultrasound assisted extraction

Conclusion

In summary, the chemical analyzes carried out with essential oil of the leaves of S. terebinthifolius indicated that δ-3-Carene was one of the major compounds (68.78%). Ferulic acid, quercetin, and caffeic acid were identified in the extracts and were considered the main substances responsible for the great antioxidant activity observed. The antimicrobial effects provide scientific basis for the popular use of S. terebinthifolius and may explain the popular use of this plant in the UTI, since

Conflict of interest

The authors report no declarations of interest.

Acknowledgments

The authors wish to thanks Tommasi Analítica Laboratory (Vila Velha, ES, Brazil) for cooperation in chromatographic analyzes and Fundação de Amparo à Pesquisa do Espírito Santo (FAPES) for the financial support.

References (40)

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