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Industrial Crops & Products 112 (2018) 70–74

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Industrial Crops & Products


journal homepage: www.elsevier.com/locate/indcrop

Short communication

Essential oil of Eucalyptus camaldulensis Dehn potentiates β-lactam activity MARK


against Staphylococcus aureus and Escherichia coli resistant strains
Thiago P. Chavesa, Raizza Eveline E. Pinheiroa, Eveny S. Meloa, Maria José dos S. Soaresb,
João Sammy N. Souzaa, Tiago Brito de Andradea, Telma Leda Gomes de Lemosc,

Henrique D.M. Coutinhod,
a
Universidade Federal do Piauí – UFPI, Campus Prof. Cinobelina Elvas – CPCE, Bom Jesus, PI, 64900-000, Brazil
b
Universidade Federal do Piauí – UFPI, Campus Ministro Petrônio Portella, Teresina, PI, 64049-550, Brazil
c
Laboratório de Biotransformação e Produtos Naturais, Universidade Federal do Ceará, Fortaleza, 60455-970, Brazil
d
Laboratório de Microbiologia e Biologia Molecular, Universidade Regional do Cariri, Crato, 63105-000, Brazil

A R T I C L E I N F O A B S T R A C T

Keywords: The emergence of multi-drug resistant bacteria is a serious worldwide health problem which has promoted the
MRSA search for strategies aimed at tackling these pathogens. Among such strategies, the development of new anti-
Bacterial resistance microbial drugs and the discovery of optimizing agents related to the existing ones stand out. This study eval-
β-lactams uated the chemical composition of the Eucalyptus camaldulensis Dehn essential oil (EOEc) and its potential as an
Essential oil
antimicrobial agent, as well as its potential a resistance modifier of β-lactamase-producing and Methicillin-
Interaction
resistant Staphylococcus aureus (MRSA) strains to β-lactam antibiotics. The EOEc was obtained through hydro-
distillation and its chemical profile through GC/MS presenting a total of five compounds with 1,8 cineole
(76.93%), β-pinene (11.49%) and α-pinene (7.15%) as its major constituents. The microdilution test was carried
out in order to determine the Minimal Inhibitory Concentration (MIC) and the bacterial resistance modulation of
the EOEc. The oil presented antimicrobial activity over the S. aureus 29 and MRSA strains
(MIC = 1000 μg mL−1). Mixtures of the essential oil and antibiotics resulted in synergistic effects, mainly with
amoxicillin and ampicillin for S. aureus 29 and MRSA, and cephalexin and cefuroxime for E. coli. The EOEc
presented antimicrobial and β-lactams optimizer potential against resistant strains, thus constituting a new
therapeutic resource against resistant bacterial strains.

1. Introduction enabling the discovery of new drugs. Used daily or with some chemical
modifications, secondary plant metabolites are present in several
The emergence and spreading of pathogenic bacteria resistant to medications which have been recently approved (Newman and Cragg,
multiple antimicrobial agents has become a large global health problem 2012).
in the XXI century (Magiorakos et al., 2012). Infections caused by these Another strategy for fighting microbial resistance is the investiga-
pathogens raise the incidence of both morbidity and mortality, as well tion of substances which may act as resistance modifiers. Several stu-
as hospitalization time and treatment costs (Laxminarayan et al., 2013). dies have assessed the association of conventional antimicrobials and
This problem is further complicated by the fact that the development of phytochemical products on multi-drug resistant bacterial strains and, in
new antimicrobials does not follow the rate at which bacterial re- most cases, synergism was observed (Chaves et al., 2016; Cristo et al.,
sistance mechanisms evolve (Lautenbach and Perencevich, 2014). In 2016; Morais-Braga et al., 2016). Such strategy could be an alternative
this sense, strategies aimed at tackling this threat are currently being to the development of new antimicrobials. Thus, the obtainment of a
sought. given medication would be faster, cheaper and carry less toxicity than
Over the centuries, natural products originating from plants have that of new antimicrobial candidate molecules (Abreu et al., 2012).
formed the basis for traditional medical systems all over the world. Species from the Eucalyptus genus have been cultivated and largely
Such substances draw the attention of researchers due to their multi- explored for many years all over the world (Luqman et al., 2008). These
plicity of applications and currently perform a fundamental role in are usually tall trees which contain a volatile essential oil that is very


Corresponding author. Universidade Regional do Cariri, Urca, Brasil, Rua Cel. Antonio Luis 1161, Pimenta, 63105−000, Brazil.
E-mail addresses: hdmcoutinho@gmail.com, hdouglas@zipmail.com.br, flavianamoraisb@yahoo.com.br (H.D.M. Coutinho).

http://dx.doi.org/10.1016/j.indcrop.2017.10.048
Received 11 June 2017; Received in revised form 24 October 2017; Accepted 29 October 2017
0926-6690/ © 2017 Elsevier B.V. All rights reserved.
T.P. Chaves et al. Industrial Crops & Products 112 (2018) 70–74

commercially important, especially for the perfumery and pharmaceu- was included as a negative control. The plates were incubated at
tical industry (Batish et al., 2006). E. camaldulensis is among the most 37 ± 1 °C for 24 h. Bacterial growth was indicated by the addition of
important species of the genus. Its leaves are used in traditional med- 20 μL of 0.01% Resazurin (Sigma–Aldrich) aqueous solution with in-
icine as an antiseptic and for the treatment of coughs and colds, sore cubation at 37 ± 1 °C for 2 h. The MIC values were identified as the
throats, diarrhea, dysentery and other infections (Bekalo et al., 2009; lowest concentration in which no bacterial growth was visible. Eva-
Al-Douri and Al-Essa, 2010; Ashraf et al., 2010). luation of the essential oil as an antibiotic resistance modulator was
The phytochemical composition of the E. camaldulensis essential oil performed according to Coutinho et al. (2010). The MIC of the anti-
has been evaluated on previous studies which found 1,8 cineole as the biotics were determined in the presence and absence of sub-inhibitory
major constituent with composition percentages ranging from 26.1 to concentrations (125 μg mL−1) of the essential oil. Plates were in-
69.46%, (Sefidkon et al., 2006; Ashraf et al., 2010; Barra et al., 2010; cubated as described above and each assay was performed in triplicates.
Medhi et al., 2010). However, different studies indicated p-cymene
(Basak and Candan, 2010) and α-pinene (Cheng et al., 2009) as the
2.4. Statistical analysis
major constituent. A large range of biological activities has also been
evaluated, such as antimicrobial (Ayepola et al., 2008; Ghalem and
The test results were expressed as the geometric mean. A Two-Way
Mohamed, 2008), larvicide (Cheng et al., 2009), cytotoxic (Al-Fatimi
analysis of variance (ANOVA) followed by Bonferroni post-hoc test was
et al., 2005), antioxidant, antidiabetic (Basak and Candan, 2010) and
applied using the GraphPad Prism 5.0 software. Only results with
anti-inflammatory activities (Bayala et al., 2014).
p < 0.05 were considered significant.
This study had as its objective to identify the chemical compounds
present in the E. camaldulensis essential oil cultivated in the northeast of
Brazil and to evaluate the properties of this oil as an antibacterial agent 3. Results and discussion
and a resistance modifier in multi-drug resistant human pathogens.
The essential oil table of chemical constituents showed a composi-
2. Materials and methods tion percentage of 80% for monoterpenes, with two of them being
oxygenates, and 20% for sesquiterpenes (Table 1). The major con-
2.1. Plant material and oil analysis stituents are presented, in descending order, by the following con-
stituents: 1,8-cineole (76.93%); β-pinene (11.49%), α-pinene (7.15%),
The essential oil extraction was carried out in the Organic Chemistry α-terpineol (2.39%) and globulol (2.04%) (Fig. 1). These results were
Laboratory at the Professora Cinobelina Elvas Campus of the Federal similar for the major component 1,8-cineole according to those re-
University of Piauí. Fresh E. camaldulensis leaves (400 g) were collected ported by Su et al. (2006).
at 12:30 h (Brasilia time) in the Bom Jesus county, Piauí state, Brazil, The chemical composition of essential oils is determined by genetic
and were subjected to hydro-distillation using Tecnal equipment, model factors, however, other factors can significantly alter the production of
TE-2761, in distilled water (500 mL). The botanical material was de- chemical constituents, including geographic localization, vegetative
posited in the herbarium Graziela Barroso − UFPI/Teresina-PI, under cycle, production method, and environmental factors, such as soil
registered number 28.835. The samples were then steam distilled for conditions, relative humidity, solar radiation, temperature and hydric
three hours. The oils obtained were analyzed by gas chromatography stress (Franco, 2005; Nascimento et al., 2006; Castro et al., 2008;
coupled to mass spectrometry (GC–MS) using a Shimadzu, QP5050A Morais, 2009).
instrument under the following conditions: dimethylpolysiloxane DB-1 Studies carried out by Jemâa et al. (2012) on the chemical com-
fused silica capillary column (30 m × 0.25 mm × 0.25 μm); carried position of E. camaldulensis essential oils in Tunisia during seasonal
gas: helium (1 mL min−1); injector temperature: 250 °C; interface variations, through the hydro-distillation method, report that the
temperature: 230 °C; split ration 27; column temperature: 35 °C–180 °C; common volatile components include 1,8-cineole, α-pinene and α-ter-
then 180 °C–250 °C; mass spectra: electron impact 70 eV. Individual pineol. Pagula et al. (2000) report that the major components of the E.
components were identified by spectrophotometric analysis using camaldulensis leaf essential oil in Mozambique were 1,8-cineole, ter-
computer library MS searches (Wiley) and Kovats indices as a pre- pinen-4-ol, α-terpineol and globulol, with the greatest variation in oil
selection aid. Visual spectra comparison data from the literature were composition being found in the monoterpenes. These data corroborate
used for confirmation (Adams, 2007). with the results found in this study concerning the chemical composi-
tion of the species being studied.
2.2. Microbial strains The EOEc presented significant antimicrobial activity over the S.
aureus strain (MIC = 1000 μg mL−1) while being inactive against E. coli
Resistant Staphylococcus aureus 29 − β-lactamase (Penicillinase) (MIC > 1000 μg mL−1). The antimicrobial activity of the E. camaldu-
producing (resistant to penicillins); S. aureus 55 (MRSA) − carrier of lensis essential oil against S. aureus and E. coli has been described in
the mecA gene (resistant to β-lactam antibiotics); and E. coli β-lacta- previous studies (Ghalem and Mohamed, 2008; Akin et al., 2010) with
mase producing (resistant to β-lactam antibiotics) strains were used.
The strains were assigned by the Microbiology Laboratory of the Table 1
Federal University of Piauí. Constituents identification of the essential oil.

CONSTITUENTS RTa (min) KIb (%)


2.3. Minimal inhibitory concentration (MIC) determination and modulation
activity α-pinene 8.264 939 7.15
β-pinene 9.729 979 11.49
1,8-cineole 11.751 1031 76.93
The minimum inhibitory concentration (MIC) was determined by α-terpineol 17.686 1188 2.39
the microdilution method in 96-well plates (CLSI, 2012) using BHI globulol 31.126 1590 2.04
broth. Microorganism colonies were suspended in 0.9% saline solution Percentage total of identificated constituents 100.00%
and the suspension was adjusted by the spectrophotometric method at Monoterpenes 4
625 nm to a final concentration of 106 CFU mL−1. Serial dilutions of the Sesquiterpenes 1
Total of the identificated constituents 5
oil solubilized in 10% DMSO in the range of 1000–3.9 μg mL−1 and
antibiotics (Cephalexin, Cefuroxime, Amoxicillin and Ampicillin) in the a
Retention Time.
range of 2500–2.4 μg mL−1 were performed. The 10% DMSO solution b
Kovats indices.

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T.P. Chaves et al. Industrial Crops & Products 112 (2018) 70–74

Fig. 1. Chromatogram of the essential oil of Eucalyptus camaldulensis.

the literature presenting several reports on the antimicrobial activity of


the compounds present in the EOEc. Studies focusing on the anti-
microbial activity of essential oils from different species attribute this
bioactivity to the compound 1,8 cineole (Carson and Riley, 1995;
Hendry et al., 2009). Other reports determined the MIC of this com-
pound on the bacteria tested in the present study with values ranging
between 8000 and 9500 μg mL−1 for S. aureus and 2400 and
8000 μg mL−1 for E. coli (Magiatis et al., 2002; Van Vuuren and Viljoen,
2007). Carson et al. (2002) evaluated the mechanism of action of the
1,8-cineole compound on S. aureus and evidenced the increase of
OD260, loss of tolerance to NaCl and morphologic changes, suggesting Fig. 2. Modulatory activity of the Essential oil of E. camaldulensis on resistance of S.
that the compound caused plasma membrane damage. aureus 55 (MRSA) to β-lactams antibiotics. *** – Statistically significant difference with
On the study carried out by Inouye et al. (2001), however, α-ter- p < 0.001; ns – not statistically significant value with p > 0.05; CFL – Cephalexin; CEF
pineol presented antimicrobial activity eight times higher than that of – Cefuroxime; AMX – Amoxicillin; AMP – Ampicillin.
1,8-cineole. Park et al. (2009) report that the antimicrobial activity of
this compound is due to its capacity to elevate the permeability to fat-
soluble compounds, while the compounds α-pinene and β-pinene are
mentioned as compounds present on essential oils with a lower effi-
ciency (Kim et al., 1995; Cosentino et al., 1999; Dorman and Deans,
2000). Nevertheless, on the study developed by Andrews et al. (1980),
α-pinene was capable of inhibiting the growth of Gram-positive, Gram-
negative and yeast microorganisms. According to the authors, the
compound caused an impairment in cell integrity and inhibited the
respiratory activity of yeast mitochondria. β-pinene provoked similar
effects on isolated mitochondria and in yeast cells, possibly acting at the
cytochrome b region from the electron transport chain (Uribe et al.,
Fig. 3. Modulatory activity of the Essential oil of E. camaldulensis on resistance of S.
1985). Moreover, α-terpineol has been presenting activity over a large
aureus 29 to β-lactams antibiotics. *** – Statistically significant difference with
spectrum of microorganisms (Park et al., 2012). Lastly, globulol also p < 0.001; ns – not statistically significant value with p > 0.05; CFL – Cephalexin; CEF
presented significant antimicrobial activity on bacterial and fungal – Cefuroxime; AMX − Amoxicillin; AMP – Ampicillin.
species (Tan et al., 2008).
The influence of the EOEc over the activity of beta-lactam anti-
(Fig. 3), respectively, were seen. Similarly, in the E. coli assays, the oil
biotics on resistant bacterial strains was also evaluated. The results
provided a significant MIC reduction for cephalexin
showed that the antibiotic combination with the EOEc enabled a re-
(26.3–17.4 μg mL−1) and cefuroxime (50.0–39.6 μg mL−1) (Fig. 4).
duction in MIC of different antimicrobial drugs over the tested strains.
β-lactam antibiotics act through the binding of penicillin-binding
On the assays using S. aureus (Fig. 2), the presence of the EOEc provided
proteins (PBPs) interfering with the synthesis and remodeling of pep-
a significant reduction in MIC for cephalexin, amoxicillin and ampi-
tidoglycans in the bacterial wall. This process leads to the formation of
cillin, with the reduction being sharper for the last two. On the S. aureus
a mechanically weaker wall which predisposes bacteria to death
55 (MRSA) assays, a reduction from 156.2 to 12.3 μg mL−1 (amox-
through cell wall lysis due to alterations in osmotic pressure (Walsh,
icillin) and 787.5 to 15.2 μg mL−1 (ampicillin) was observed. Mean-
2000). The resistance mechanisms of these antibiotics include (1)
while, with the S. aureus 29 assays, a reduction from 248.0 to
substituting the present PBPs for others with lower drug affinities; (2)
6.1 μg mL−1 and 625.0 to 9.7 μg mL−1 for amoxicillin and ampicillin
production of β-lactamase, which deactivates the β-lactams from the

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