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Vol. 10(48), pp. 865-871, 25 December, 2016
DOI: 10.5897/JMPR2016.6291
Article Number: C9CCEE862182
ISSN 1996-0875
Copyright © 2016
Author(s) retain the copyright of this article
http://www.academicjournals.org/JMPR
Journal of Medicinal Plants Research
Full Length Research Paper
Chemical composition and antifungal activity of
essential oil and fractions extracted from the leaves of
Laurus nobilis L. cultivated in Southern Brazil
Carla M. M. Fernandez-Andrade1, Maurício F. da Rosa1, Édela Boufleuer1, Fabiana Borges
Padilha Ferreira2, Camila Cristina Iwanaga2, José E. Gonçalves3, Diógenes A. G. Cortez4,
Cleide Viviane Buzanello Martins1, Giani Andrea Linde5, Márcia R. Simões1, Viviane S. Lobo6
and Zilda C. Gazim5*
1Postgraduate Program in Pharmaceutical Sciences, State University of Western Paraná, Cascavel, Paraná, Brazil.
2Postgraduate Program in Pharmaceutical Sciences, State University of Maringá, Maringá, Paraná, Brazil.
3Postgraduate Programs in Clean Technologies and Health Promotion, Cesumar University, Maringá, Paraná, Brazil.
4Postgraduate Programs in Health Promotion, Cesumar University, Maringá, Paraná, Brazil.
5Postgraduate Program in Biotechnology Applied to Agriculture, Paranaense University, Umuarama, Paraná, Brazil.
6Postgraduate Program in Chemical Technologies and Biochemical Processes, Federal Technological University of
Parana, Brazil.
Received 4 November, 2016; Accepted 14 December, 2016
Laurus nobilis L., popularly known as laurel, is a tree belonging to the Lauraceae family, native to Asia.
It has long been used in traditional medicine to treat rheumatic disorders, and as a gastric stimulant.
The aim of this study was to characterize the chemical composition of essential oils (EO) and fractions
from laurel by column chromatography, and to evaluate their antifungal activity. The EO of L. nobilis
leaves was obtained by hydrodistillation, and separated by column chromatography. Thirty-two EO
constituents were identified, with 1,8-cineole and linalool comprising 40.14 and 15.69% of the total yield,
respectively. The major constituents of the fractions (FR) were: α-terpinyl acetate (FR1: 52.65%), 1,8-
cineole (FR2: 76.88%), 1,8-cineole (FR3: 84.24%), linalool (FR4: 67.26%), and linalool (FR5: 90.64%).
Antifungal activity of EO and fractions were tested by a broth microdilution method, whereby minimum
inhibitory concentration (MIC) was determined against several fungal organisms (Candida albicans,
Candida krusei, Candida parapsilosis, Candida tropicalis, Cryptococcus gattii, and Cryptococcus
neoformans). EO showed moderate inhibition of C. neoformans (MIC 0.62 mg/mL), and strongly
inhibited of C. gattii (MIC 0.31 mg/mL). FR3 moderately inhibited C. neoformans (0.62 mg/mL), and
strongly inhibited C. gattii (MIC 0.31 mg/mL). FR5 moderately inhibited strains of C. gattii and C.
neoformans (MIC 0.62 mg/mL). Laurel´s EO and the fractions analyzed in this study were confirmed to
have antifungal properties. However, further studies on toxicity of these substances and in vivo
experiments are necessary to confirm the results presented herein.
Key words: Laurus nobilis, antifungal, linalool, 1,8-cineole.
INTRODUCTION
Infectious diseases caused by fungi are responsible for
morbidity and mortality in thousands of hospitalized and immune compromised individuals annually (Lemke et al.,
2005; Alangaden, 2011). Therefore, the development of
novel antifungal drugs is of vital importance. Patients with
human immunodeficiency virus infection (HIV infection/
AIDS) comprise a highly susceptible group, and the
number of opportunistic infections reported for this group
has increased dramatically (Omoruyi et al., 2014).
Cryptococcosis, a systemic mycosis caused by yeasts of
the Cryptococcus genus, most commonly Cryptococcus
gattii and Cryptococcus neoformans, is the third most
prevalent disease in people with HIV infection/ AIDS
(Gullo et al, 2013; Maziarz and Perfect, 2016). These
agents are responsible for cryptococcal meningitis, a
disease most commonly diagnosed in sub-Saharan
Africa, where it may kill more people each year than
tuberculosis. Globally, one million new cases of
cryptococcosis are estimated to occur in HIV-positive
individuals annually, resulting in nearly 624,700 deaths,
most due to meningitis (Park et al., 2009).
Additionally, the Candida yeasts are of clinical
importance, causing opportunistic infections. Candidemia
(disseminated hematogenous infection) or deep-seated
infection in normally sterile body sites of
immunosuppressed patients cause high morbidity and
mortality, and also increase medical costs by increasing
the duration of hospitalization (Patterson, 2005;
Alangaden, 2011; Menezes et al., 2012). C. albicans is
one of the major causes of infection of skin and mucosal
surfaces, it can infect any organ and in cases of
infections in the bloodstream can lead to death, if left
untreated (Noble and Johnson., 2007; Duggan et al.,
2015). Another species of great importance is C.
parapsilosis, which has recently emerged as the second
most commonly isolated species in candidemia, infects
groups such as neonates, transplant patients, and
individuals receiving parenteral nutrition. C. parapsilosis
has the ability to form biofilms with high affinity for
intravascular and parenteral nutrition devices, being more
prevalent than C. albicans in patients using such devices
(Trofa et al., 2008; Menezes et al., 2012). C. tropicalis is
increasingly isolated from patients with hematologic
malignancies, and its presence is predictive for infection
causing mucositis and neutropenia. C. krusei is the fifth
most common species in immunocompromised patients,
with high mortality rates because of resistance to
commonly used antifungal drugs such as fluconazole
(Pfaller et al., 2008; Sipsas et al., 2009; Alangaden, 2011).
Microbial resistance develops through naturally
occurring mutations in fungal cells during prolonged
antifungal treatment, resulting in selection of the most
resistant strain (Pfaller, 2012). Resistance to drugs is a
major concern worldwide because of the limited number
of antifungal drug classes, and because the number of
patients requiring antifungal treatment is increasing
Fernandez-Andrade et al. 866
(Maubon et al., 2014). Because of the pressing need for
novel therapies to treat the fungal infections, researchers
have directed their studies toward the discovery of
natural substances with greater efficacy and lower toxicity
(Pina et al., 2012; Santos and Novales, 2012).
Secondary metabolism in plants produces many
compounds that have complex chemical structures, many
of these substances have been reported to have
antimicrobial properties as essential oils (EOs) (Edris,
2007). EOs are important natural products, being
multifunctional, well accepted by consumers, and safer
than synthetic additives. Thus, they have been targeted
for research on natural food preservation, crop protection,
pharmaceutical applications, and cosmetic production
(Bakkali et al., 2008; Okoh et al., 2010).
Laurus nobilis L. is a tree belonging to the Lauraceae
family, native to Asia. The plant is popularly known as
laurel, and is cultivated in south and southeast Brazil
(Marques, 2001; Lorenzi and Matos, 2008). Laurel is an
aromatic spice, commonly used to season recipes owing
to its aroma. Laurel leaf is also used in folk medicine as
infusions or decoctions, being considered a gastric
stimulant as well as a treatment for rheumatic disorders.
It is also used externally for rheumatism, and as an
antiseptic for dandruff and lice (Joly, 1993; Marques,
2001; Lorenzi and Matos, 2008).
Laurel leaves are widely used in the food, cosmetic,
and perfumery industries, and their essential oil (EO) is
highly valued. Large amounts of phytoactive agents are
found in EO among which is terpenes. The EO are widely
studied, and their antibacterial (Angelini et al., 2006),
antifungal (Gumus et al., 2010), antioxidant (Inan et al.,
2012), insecticidal (Sertkaya et al., 2010), antiproliferative
(Abu-Dahab et al., 2014), analgesic, and anti-
inflammatory properties (Sayyah et al., 2003) reported.
This present study was designed to evaluate the
antifungal activity of EO and fractions extracted from the
leaves of L. nobilis cultivated in Southern Brazil.
MATERIALS AND METHODS
Plant material
Fresh leaves of L. nobilis L. were collected in January 2014, in the
city of Pérola, Paraná, Brazil (23º 50’ 56.6” S 53º 41’ 06.2” W, 20
m), identified by Msc. Mayara Lautert and Camila Vanessa Buturi,
as sample number 1615, and were deposited at the Herbarium of
the State University of Western Paraná.
Essential oil extraction
Fresh leaves of L. nobilis L. were subjected to hydrodistillation in a
*Corresponding author. E-mail: cristianigazim@unipar.br. Tel: +554499679382, +554436212837 Fax: +554436212849.
Author(s) agree that this article remain permanently open access under the terms of the Creative Commons Attribution
License 4.0 International License
867 J. Med. Plants Res.
apparatus for 2 h (Fiorini et al., 1997). EO was collected, dried over
sodium sulfate, filtrated, and stored in amber-colored vials at 4°C.
After total evaporation of the solvent, the EO was weighed to
calculate oil yield (%).
Obtaining L. nobilis EO fractions
EO (4.0 g) was submitted to silica gel column chromatography and
eluted sequentially with n-hexane, dichloromethane, ethyl acetate,
methanol, and hexane: dichloromethane (9:1; 8:2; 7:3, and 5:5 v/v),
dichloromethane: ethyl acetate (9:1, 8:2, 7:3, and 5:5 v/v), and ethyl
acetate: methanol (9:1, 8:2 , 7:3, and 5:5 v/v) mixtures. The
fractions were then concentrated under reduced pressure using a
rotary evaporator (Tecnal TE-211) to reduce the volume to about
2.0 mL, transferred to amber vials, dried, and stored at 4ºC for the
duration of the experiment.
GC-MS analysis
Analysis of EO was carried out in a gas chromatograph (Agilent
7890 B) coupled to a mass spectrometer (Agilent 5977 A) equipped
with an Agilent HP-5MS capillary column (30 m × 0.250 mm × 0.25
μm), using the following conditions: injector temperature of 250°C,
injection volume 1 μL at a ratio of 1:30 (split mode), initial column
temperature of 50°C, heated gradually to 260°C at 3°C/min rate.
The carrier gas (helium) flow was set at 1 mL/min. The
temperatures of the transfer line, ion source, and quadrupole were
250, 230 and 150°C, respectively (Derwich et al., 2009; Moghtader
and Salari, 2012). Mass spectra were obtained with a scan range of
40 to 500 m/z and a solvent delay time of 3 min, and compounds
were identified based on comparison of their retention indices (RI),
obtained using various n-alkanes (C8-C25). In addition, their
electron ionization (EI) mass spectra were compared with the NIST
11.0 library spectra according to Adams (2007).
Determination of the minimum inhibitory concentration (MIC)
Minimum inhibitory concentrations (MIC) of EO were determined
against C. albicans ATCC 18804, C. krusei ATCC 20298, C.
parapsilosis ATCC 20019, C. tropicalis ATCC 750, C. gattii L21/01,
and C. neoformans H99. An 80 mg/mL of the EO solution was
prepared, diluted with 2% polysorbate 80 (tween 80) in Muller
Hinton Broth with the addition of 2% glucose for yeasts. The culture
medium (100 μL) was distributed into the wells of a microdilution
plate, and then 200 μL EO solution was added to the second well.
Following homogenization, this was transferred to the third well,
and so on until the tenth. Thus, the final concentrations obtained
were 40.00, 20.00, 10.00, 5.00, 2.50, 1.25, 0.62 and 0.31 mg/mL. A
microbial suspension was prepared in saline with turbidity
equivalent to 0.5 on the McFarland scale (1 × 108 UFC/mL). Next,
the 1:50 yeast suspension was diluted to 1:20 in Mueller Hinton
Broth modified for fungi to yield 1 × 105 UFC/mL inoculums.
Hundred microliters of the suspensions was inoculated in triplicate
into each well containing the various EO concentrations. Well 1 was
used as sterility control. The toxicity control was well 11 with 2%
polysorbate 80 in culture medium. Well 12 was used as the growth
control, where microbial suspension was added to the culture
medium. Microplates were incubated at 35°C for 24 h in aerobic
conditions. MICs were determined by examining the plates. The
lowest concentration of EO causing complete inhibition of growth
(CLSI, 2008) was reported. The same procedure was performed
with fractions of the essential oil, using an initial solution of 20
mg/ml and the fluconazole was used as positive control.
Statistical analysis
The data were subjected to analysis of variance (ANOVA) and
comparisons of means by Tukey’s test at a 5% significance level.
RESULTS AND DISCUSSION
Hydrodistillation of laurel leaves resulted in a 0.66% yield
of EO. The yield obtained is in accordance with that
reported by Lira et al. (2009), who obtained a yield
between 0.3 and 1.2% during their 15-month study.
Thirty-two different constituents were identified (Table
1). The majority were terpenoids (93.50%), followed by
phenylpropanoids (6.04%). The major terpenoid
constituents obtained were monoterpene hydrocarbons
(14.44%), oxygenated monoterpenes (78.15%),
sesquiterpene hydrocarbons (0.69%) and oxygenated
sesquiterpenes (0.21%). Oxygenated monoterpenes form
the majority of the EO, 1,8-cineole being the predominant
component (40.14%), followed by linalool (15.69%), and
α-terpinyl acetate (11.70%). Sellami et al. (2011) also
reported 1,8-cineole (61.17%) to be the major compound
in samples of fresh laurel leaf EO, and Moghtader and
Salari (2012) showed that the EO of dried laurel leaves
contained 25.7% 1,8-cineole.
Silveira et al. (2012) analyzed the EO of laurel
cultivated in Concordia (Santa Catarina - Brazil) by GC-
MS. The authors observed that the oil contained 1,8-
cineole (35.50%) as its major constituent, followed by
linalool (14.10%), α-terpinyl acetate (9.65%), and
sabinene (9.45%). The results of the present work are in
line with those reported by these authors. In Croatia,
Politeo et al. (2006) reported the major compounds in
laurel EO to be 1,8-cineole (34.9%), linalool (13.5%),
methyl eugenol (13.5%), and α-terpinyl acetate (12.2%).
Dadalioglu and Evrendilek (2004) analyzed the EO of
fresh L. nobilis leaves collected in Hatay, Turkey, and
found the major constituents to be 1,8-cineole (60.72%),
α-terpinyl acetate (12.53%), and sabinene (12.12%). The
differences in the chemical composition of EO of laurel
can be attributed to plant origin, time of harvesting, drying
processes, and other factors such as climate, soil,
vegetative stage, and processing (extraction) (Simões
and Spitzer , 2007).
The fractions tested were identified by GC-MS. The
fractions (FR) were characterized as follows: FR1;
dichloromethane: hexane (7:3) fraction composed of α-
terpinyl acetate (52.65%), 1,8-cineole (29.70%), eugenol
(4.28%), and methyl eugenol (9.52%); FR2;
dichloromethane: hexane (8:2) fraction composed of 1,8-
cineole (76.88%), methyl eugenol (21.07%), α-terpinyl
acetate (1.28%), and eugenol (0.77%); FR3;
dichloromethane: hexane (9:1) fraction composed of 1,8-
cineole (84.24%) and linalool (6.78%); FR4;
dichloromethane fraction composed of 67.26% linalool
and 1,8-cineole (19.68%); and FR5; dichloromethane:
ethyl acetate (9:1) fraction composed of 90.64% linalool
Fernandez-Andrade et al. 868
Table 1. Chemical composition of essential oil and fractions obtained from the leaves of Laurus nobilis.
Peak
Constituent*
RI**
% Area
Identification methods
1
α-Thujene
931
0.25
a,b
2
α-Pinene
937
2.53
a,b
3
Camphene
952
0.05
a,b
4
Sabinene
978
5.71
a,b
5
β-Pinene
981
2.36
a,b
6
β-Myrcene
997
0.32
a,b
7
δ-2-Carene
1010
0.03
a,b
8
α-Phellandrene
1015
0.14
a,b
9
α-Terpinene
1021
0.23
a,b
10
ο-Cymene
1029
0.37
a,b
11
Limonene
1033
1.57
a,b
12
1,8-Cineole
1035
40.14
a,b
13
(E)-β-Ocimene
1053
0.03
a,b
14
γ-Terpinene
1063
0.61
a,b
15
cis-Sabinene hydrate
1071
0.36
a,b
16
Terpinolene
1094
0.17
a,b
17
n.i.
1104
0.34
a,b
18
Linalool
1106
15.69
a,b
19
cis-ρ-Menth-2-en-1-ol
1126
0.08
a,b
20
δ-Terpineol
1172
0.36
a,b
21
Terpinen-4-ol
1182
3.17
a,b
22
α-Terpineol
1195
6.22
a,b
23
n.i.
1234
0.13
a,b
24
Linalool acetate
1263
0.08
a,b
25
δ-Terpinyl acetate
1323
0.42
a,b
26
α-Terpinyl acetate
1355
11.70
a,b
27
Eugenol
1363
0.20
a,b
28
β-Elemene
1397
0.21
a,b
29
Methyl eugenol
1411
5.84
a,b
30
(E)-Caryophyllene
1424
0.44
a,b
31
γ-Cadinene
1529
0.04
a,b
32
Caryophyllene oxide
1587
0.21
a,b
Compound groups (%)
Monoterpene hydrocarbons
14.44
Oxygenated monoterpenes
78.15
Sesquiterpene hydrocarbons
0.69
Oxygenated sesquiterpenes
0.21
Phenylpropanoids
6.04
Total of identified compounds
99.54
*Compounds listed in order of elution from HP-5MS column; **RI = Retention index; aIdentification based on RI; bIdentification based on
comparison of mass spectra; n.i. = not identified.
as the major constituents.
The results for MIC tests of EO and fractions are
presented in Table 2. In order to compare the results, the
values found in this study were compared with the
classification values proposed by Aligiannis et al. (2001)
and Duarte et al. (2005) for plant materials, based on
MIC results. This classification system categorizes
materials as strong inhibitors; MIC up to 0.5 mg/mL,
moderate inhibitors; MIC between 0.6 and 1.5 mg/mL,
and weak inhibitors; MIC above 1.6 mg/mL. In the
present study, EO demonstrated low inhibition of Candida
strains, moderate inhibition of C. neoformans (MIC 0.62
mg/mL), and high inhibition of C. gattii (MIC 0.31 mg/mL).
FR1 moderately inhibited C. gattii (MIC 1.25 mg/mL).
FR3 moderately inhibited C. krusei (MIC 1.25 mg/mL)
and C. neoformans (MIC 0.62 mg/mL), and strongly
869 J. Med. Plants Res.
Table 2. Minimum inhibitory concentration (MIC) of essential oil and fractions of L. nobilis (mg/mL).
Microorganisms
Essential oil of laurel
FR 1
FR 2
FR 3
FR 4
FR 5
Candida albicans
5.00b
>10.00a
>10.00a
>10.00a
1.25c
1.25c
Candida krusei
10.00b
>10.00a
>10.00a
1.25d
2.50c
2.50c
Candida parapsilosis
5.00b
>10.00a
>10.00a
>10.00a
5.00b
2.50c
Candida tropicalis
10.00b
>10.00a
>10.00a
>10.00a
1.25c
1.25c
Cryptococcus gattii
0.31d
1.25b
5.00a
0.31d
1.25b
0.62c
Cryptococcus neoformans
0.62d
>10.00a
5.00b
0.62d
1.25c
0.62d
FR1: Dichloromethane:hexane: (7:3) was composed of α-terpinyl acetate (52.65%), 1,8-cineole (29.70%), eugenol (4.28%), and methyl eugenol
(9.52%); FR2: Dichloromethane:hexane (8:2) of 1,8-cineole (76.88%), methyl eugenol (21.07%),α-terpinyl acetate (1.28%), and eugenol (0.77%); FR3:
Dichloromethane:hexane (9:1) of 1,8-cineole (84.24%) and linalool (6.78%); FR4: Dichloromethane of linalool (67.26%) and 1,8-cineole (19.68%);
FR5: Dichloromethane:ethyl acetate (9:1) of 90.64% of linalool as the major constituents. Values are the mean ± standard deviation of the experiment
performed in triplicate. Different letters in the same line are different (p≤0.05) by Tukey’s test.
inhibited C. gattii (MIC 0.31 mg/mL). FR4 moderately
inhibited C. albicans, C. tropicalis, C. gattii and C.
neoformans (MIC 1.25 mg/mL). FR5 moderately inhibited
C. albicans and C. tropicalis (MIC 1.25 mg/mL), C. gattii
and C. neoformans (MIC 0.62 mg/mL). Both FR4 and
FR5 slightly inhibited C. krusei and C. parapsilosis.
Studies carried out by Erturk et al. (2006) showed the
antifungal activity of laurel EO against C. albicans, with
an MIC of 2.4 mg/mL. Peixoto et al. (2017) evaluated the
antifungal activity of EO of laurel collected in Brazil, and
found isoeugenol (53.5%) and myrcene (16.6%) as major
constituents. The EO showed activity against C. albicans
strains (MIC 0.25 mg/mL), C. tropicalis (MIC 0.50 and
0.25 mg/mL), C. krusei and C. glabrata (MIC 0.5 mg/mL).
The EO evaluated in the present study exhibited a higher
MIC (10.00 and 5.00 mg/mL) for Candida strains; the
differences in biological activities between these findings
and the literature may be attributable to the differences in
chemical composition of EO of laurel that directly
influences its antimicrobial activity.
Monoterpenes and sesquiterpenes with aromatic rings
and phenol groups are capable of forming hydrogen
bonds with the active sites of target enzymes, and this is
the main mode of antimicrobial action of EO. Other
compounds such as alcohols, aldehydes, and esters also
contribute to antimicrobial activity (Belletti et al., 2004).
The antifungal activity of the fractions can be attributed to
the presence of terpenes. Linalool, the major constituent
in FR 4 and FR5, was screened for activity against
Candida isolates by Marcos-Arias et al. (2011), who
reported findings against C. albicans (MIC, 0.30-2.50
mg/mL), C. tropicalis (0.60-2.50 mg/mL), C. parapsilosis
(0.30 mg/mL), and C. krusei (0.60 mg/mL). The eugenol
in FR1 and FR2, and terpinen-4-ol present in FR3–5
were also investigated by Marcos-Arias et al. (2011);
against C. albicans eugenol had an MIC in the range of
0.60-2.50 mg/mL, and terpinen-4-ol in the range of 0.60-
5.00 mg/mL; for C. tropicalis, the eugenol and terpinen-4-
ol MIC range was 0.60-1.20 mg/mL; for C. parapsilosis,
the MIC of both substances was 0.60 mg/mL; and for C.
krusei, both had an MIC of 1.20 mg/mL. In general, the
MIC values reported for the fractions in this study against
Candida species are close to those found by Marcos-
Arias et al. (2011), considering that they evaluated pure
substances, while the fractions in this present study are a
mixture of terpenes, which may or may not have
synergistic effects. Hsu et al. (2013) determined the MIC
against Candida species for linalool, and found it to
be1.23 to 4.93 mg/mL for C. albicans, and 2.47 mg/mL
for C. tropicalis. These values are comparable to those
found in the present study for FR4 and FR5, in which
linalool is the major compound.
1,8-Cineole is present in all fractions, and is the major
compound in FR2 and FR3 (76.88 and 84.24%,
respectively); its antifungal activity was investigated by
Adegoke et al. (2000) against Candida tropicalis yeast. It
was found to have an MIC of 0.16 mg/mL against C.
tropicalis yeast, with an activity superior to the that
recorded for the fractions containing 1,8-cineole in the
present study. However, these authors investigated the
use of pure substances. Hammer et al. (2003)
determined the MIC for 1,8-cineole against isolates of C.
albicans (40.00 mg/mL) and C. parapsilosis (80.00
mg/mL). Pattnaik et al. (1997) analyzed the antifungal
action of oxygenated linalool and 1,8-cineole
monoterpenes, and found linalool to possess activity
against C. albicans (MIC 0.20 mg/mL). C. albicans was
resistant to 1,8-cineole at MIC up 5.00 mg/mL. This
present study documented lower linalool activity in the
fractions containing it as the major compound. Fractions
containing 1.8-cineole had higher antifungal activity
against C. albicans and C. parapsilosis in comparison
with the results of the studies mentioned above; this may
be explained by the fact that fractions are a mixture of
antifungal substances acting in synergy.
To our knowledge, this is the first investigation
documenting antifungal activity of EO and fractions
extracted from fresh leaves of laurel against strains of C.
parapsilosis, C. gattii, and C. neoformans. EO extracted
and analyzed in this study, as well as its fractions,
possess antifungal properties. The presence and
proportion of the EO constituents are related to biological
properties of laurel. However, further studies on toxicity of
these substances and in vivo experiments are necessary
to confirm the results here presented.
Conflicts of Interests
The authors have not declared any conflict of interests.
ACKNOWLEDGEMENTS
The authors acknowledge financial support by the
Coordination for Improvement of Higher Education
Personnel (Coordenação de Aperfeiçoamento de
Pessoal de Nível Superior - CAPES).
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