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Residues from the Brazilian Pepper Tree (Schinus Terebinthifolia Raddi

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Residues from the Brazilian Pepper Tree (Schinus Terebinthifolia Raddi Industrial Crops & Products 143 (2020) 111430 Contents lists available at ScienceDirect Industrial Crops & Products journal homepage: www.elsevier.com/locate/indcrop Residues from the Brazilian pepper tree (Schinus terebinthifolia Raddi) T processing industry: Chemical profile and antimicrobial activity of extracts against hospital bacteria ⁎ Rodrigo Borges de Araujo Gomesa,b, , Erica Santana de Souzac, Nataly Senna Gerhardt Barraquid, Cristina Luz Tostaa, Ana Paula Ferreira Nunesc, Ricardo Pinto Schuenckc, Fabiana Gomes Ruase, ⁎ José Aires Venturae, Paulo Roberto Filgueirasa, Ricardo Machado Kustera, a Laboratório de Cromatografia, Departamento de Química, Universidade Federal do Espírito Santo, Vitória, ES, Brazil b Instituto Federal do Espírito Santo – IFES, Aracruz, ES, Brazil c Programa de Pós-Graduação em Doenças Infecciosas, Universidade Federal do Espírito Santo, Vitória, ES, Brazil d Programa de Pós-Graduação em Biologia Vegetal, Universidade Federal do Espírito Santo, Vitória, ES, Brazil e Instituto Capixaba de Pesquisa, Assistência Técnica e Extensão Rural – Incaper, Vitória, ES, Brazil ARTICLE INFO ABSTRACT Keywords: Schinus terebinthifolia Raddi is a plant used in folk medicine in the treatment of various diseases and has several Schinus terebinthifolia biological potentials. Its fruit is used as condiment and has high demand in the spice market. In the present study Brazilian pepper tree extracts of different polarities prepared from residues from the Brazilian pepper tree processing industry were Residues characterized chemically by gas chromatography/mass spectrometry (GC–MS) and negative-ion mode electro- Antimicrobial activity spray ionization Fourier transform ion cyclotron resonance mass spectrometry (ESI(-)FT-ICR MS). The anti- Phenolic compounds bacterial activity of the extracts was evaluated against multidrug-resistant strains of hospital origin (Staphylococcus aureus, Enterococcus faecium, Enterococcus faecalis, Pseudomonas aeruginosa and Acinetobacter baumannii) and standard strains (ATCC). The apolar fractions (dichloromethane and hexane) presented tri- terpenes as main components and the polar extracts (methanol and hydroethanolic extracts) were characterized by high contents of phenolic compounds, especially gallotannins, gallic acid and flavonoids. The methanolic fraction and the hydroethanolic extract of the residues were the most active mainly against S. aureus (MIC 0.60–0.90 mg/mL), E. faecium and E. faecalis (MIC 1.20–2.10 mg/mL). These results demonstrate the richness of bioactive compounds present in the residues and indicate a possible application of this material for the devel- opment of biotechnological products with potential against multidrug-resistant bacteria. 1. Introduction addition to being used in food industry, S. terebinthifolia is also widely used in folk medicine due to its different biological activities, such as Schinus terebinthifolia Raddi (Syn.: Schinus terebinthifolius Raddi) anti-allergic (Cavalher-Machado et al., 2008), anti-inflammatory (Rosas (Anacardiaceae), is known as Brazilian pepper tree or aroeira. It is a et al., 2015; da Silva et al., 2017b) and antimicrobial (Gomes et al., species widely distributed along the Brazilian coast (Morton, 1978; 2013; Muhs et al., 2017; da Silva et al., 2017a). Phytochemical studies Carvalho et al., 2013). Its fruits are used as condiment and have high have described the presence of gallic acid, methyl gallate, ethyl gallate, demand in the international market. In Brazil a large part of the fruit flavonoids myricitrin, myricetin and quercitrin (Ceruks et al., 2007; production originates from the extractive exploitation, mainly in Santana et al., 2012), anthocyanins, bioflavonoids, hydrolyzable tan- Espírito Santo and Rio de Janeiro states. Currently, some producers in nins such as galloylglucose and galloyl shikimic acids (Feuereisen et al., the state of Espírito Santo have been growing aroeira (rose pepper) for 2014, 2017). This species is present in the Phytotherapeutic Form of the the international market due to high prices reached in this agribusiness Brazilian Pharmacopoeia (2011) (Anvisa, 2011) and in the list of phy- (Neves et al., 2016). Therefore, Espírito Santo has become one of the totherapics of the National Relation of Essential Medicines (Brazilian most important Brazilian state for that agricultural production. In Ministry of Health, 2017). ⁎ Corresponding authors at: Laboratório de Cromatografia, Departamento de Química, Universidade Federal do Espírito Santo, Vitória, ES, Brazil. E-mail addresses: [email protected], [email protected] (R.B.d.A. Gomes), [email protected] (R.M. Kuster). https://doi.org/10.1016/j.indcrop.2019.05.079 Received 7 January 2019; Received in revised form 24 May 2019; Accepted 27 May 2019 Available online 05 June 2019 0926-6690/ © 2019 Elsevier B.V. All rights reserved. R.B.d.A. Gomes, et al. Industrial Crops & Products 143 (2020) 111430 Bacterial resistance is considered a global public health problem. spectrometry (GC–MS) on an Agilent 7890B (Agilent, California, USA) Infections caused by bacteria resistant to antibiotics are associated with equipped with an HP-5MS column (30 m × 0.25 mm, film thickness excess mortality, prolonged hospitalization and increased hospital costs 0.25 μm) and an Agilent 5977A MSD mass detector. The initial column (Cosgrove, 2006; de Kraker et al., 2011). Therefore, control initiatives temperature was set at 40 °C, remaining for 1 min. Thereafter, a heating have been proposed in the attempt to combat infections caused by re- rate of 5 °C/min was used up to 240 °C, increased to 310 °C at 30 °C/min sistant microorganisms. In 2017 the World Health Organization re- and maintained for 20 min. The total analysis time was 63 min. The leased a list of priority pathogens for research and development of new carrier gas was helium at a flow rate of 1 mL/min. Injector and detector antibiotics. Among them are methicillin-resistant Staphylococcus aureus temperatures were set at 290 °C and 310 °C, respectively. The MS was (MRSA), vancomycin-resistant Enterococcus faecium (VRE), Acineto- operated in electron impact ionization mode (70 eV, 50–500 Da). The bacter baumannii and Pseudomonas aeruginosa resistant to carbapenem samples were diluted in hexane (5.8 mg/mL) and dichloromethane (WHO, 2017). This information demonstrates the importance and the (10 mg/mL) and the injected volume was 1.0 μL with the injector in concern with the development of research on active agents against the split mode 1:10. A series of n-alkanes was analyzed under the same strains of these microorganisms. Considering the potential of S. ter- chromatographic conditions for the calculation of the retention index of ebinthifolia Raddi as an antimicrobial plant of popular use, the high the substances. The main chemical constituents of the samples were availability of raw material (residues) and the need for research in- proposed by comparing the mass spectra with the NIST library data volving these pathogens, this work aimed to characterize the residues base, afterwards by comparing the retention indices to the literature from the Brazilian pepper tree processing industry and to evaluate its (Adams, 2009; The Pherobase-Database, 2018; Chemistry WebBook, activity against multidrug-resistant bacteria. 2018). 2. Material and methods 2.5. ESI(-)FT-ICR MS and ESI(-)FT-ICR MS/MS analyses 2.1. Plant material The methanolic, dichloromethane and hydroethanolic extracts were analyzed by Fourier Transform Ion Cyclotron Mass Spectrometry (FT- The residues were collected in an industry located in the munici- ICR MS) to determine the chemical profile. The samples were solubi- pality of Boa Esperança - ES, which receives fruits produced in the south lized (1 mg/mL) in a solution of acetonitrile:water (1:1) which was and in the north of Espírito Santo under cultivation guidance by the infused at a rate of 5 μL/min in the negative mode operated electro- Capixaba Institute of Research, Technical Assistance and Rural spray (ESI) source. The mass spectrometer (model 9.4 T Solarix, Bruker Extension (Incaper). This material is composed mostly of leaves and Daltonics, Bremen, Germany) was set to operate over a range of m/z minority of unusable fruits. Another material composed exclusively of 150–1500. Among the ESI source conditions used in the analyzes are the fruit peels discarded in the process was also collected for the pre- the nebulizer gas pressure of 1.0 bar, the capillary voltage of 3.8 kV and paration of extracts. the capillary transfer temperature of 200 °C. In addition, the accumu- lation time of the ions was 0.010 s and each spectrum was acquired by 2.2. Preparation of the extracts accumulating 32 scans of time-domain transient signals in 16 mega- point time-domain data sets. The tandem mass spectrometry (MS2) 2.2.1. Extraction of Brazilian pepper tree residues (leaves and fruits) experiments were performed on a quadrupole analyzer coupled to the The extracts were prepared by subjecting the sample (50 g) to the FT-ICR mass spectrometer. The MS2 spectra were acquired using the ion organic solvents hexane (HF) (3 × 130 mL), dichloromethane (DF) accumulation time of 1 s, isolation window of 1.0 (m/z units) and (3 × 130 mL) and methanol (MF) (3 × 130 mL) successively. At each 25–45% of the collision energy. The mass spectra were acquired and extraction, in the maceration mode, the solvent remained in contact processed using Data Analysis software (Bruker Daltonics, Bremen, with the sample for
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