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Antibacterial activity of Nigella sativa L.seed oil in water emulsion against

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Gasong et al., IJPSR, 2017; Vol. 8(7): 3155-3161. E-ISSN: 0975-8232; P-ISSN: 2320-5148

IJPSR (2017), Volume 8, Issue 7 (Research Article)

Received on 29 December, 2016; received in revised form, 17 March, 2017; accepted, 21 March, 2017; published 01 July, 2017

ANTIBACTERIAL ACTIVITY OF NIGELLA SATIVA L. SEED OIL IN WATER EMULSION

AGAINST DENTAL CARIOGENIC BACTERIA
Beatrix T. Gasong, Apriliana W. Hartanti and Raymond R. Tjandrawinata *
Dexa Laboratories of Biomolecular Sciences (DLBS), PT Dexa Medica, Industri Selatan V Block PP no.
7, Jababeka Industrial Estate II, Cikarang - 17550, West Java, Indonesia.
Keywords: ABSTRACT: Our previous study highlighted the antimicrobial activity
Nigella sativa, Oil-in-water emulsion,
evaluation of Nigella sativa seed oil extract that was obtained from supercritical
Antimicrobial, Dental cariogenic fluid extraction using carbon dioxide (SCFE-CO2) on Gram positive pathogenic
bacteria bacteria. The aim of this study was to formulate oil-in-water (o/w) emulsion of
Correspondence to Author: previous N. sativa seed oil extract and to investigate its antimicrobial activity
Raymond R. Tjandrawinata against Streptococcus mutans and Streptococcus sanguis as the most common
causative bacteria of dental caries. Oil-in-water emulsion containing 10% N.
Dexa Laboratories of Biomolecular sativa seed oil extract (DLBS1355) exhibited good inhibition activity on both S.
Sciences (DLBS), PT Dexa Medica, mutans and S. sanguis. Time-kill assay and biofilm inhibition assay were
Industri Selatan V Block PP no. 7, conducted using emulsion with 0.5% N. sativa seed oil extract content. The
Jababeka Industrial Estate II, results showed bactericidal and biofilm inhibition activities on both tested
Cikarang - 17550, West Java,
bacteria. Antimicrobial activity of the emulsion was found higher on S. sanguis
Indonesia.
than S. mutans. Results of the present study showed that emulsification process
Email: [email protected] did not significantly affect the antimicrobial activity of N. sativa seed oil extract
and the formulated N. sativa oil-in-water emulsion could further be used as an
antimicrobial agent against dental cariogenic bacteria.
INTRODUCTION: Dental caries and dental The potency of some Indonesian medicinal plants
periodontitis are the most common dental- has been widely highlighted by several studies for
associated diseases especially in Asian countries. their therapeutic effect as anti-inflammatory,
Compared to other Asian countries, Indonesia has anticancer, hepatoprotector, and antidiabetic. 8-11
higher prevalence of dental caries in children.1 The Natural-based remedies have also been recently
prevalence of dental caries in Indonesia was recommended to substitute the uses of fluoride and
increased about 10% in 2007-2013 that was other chemical compounds addressed for oral
predicted due to social economy factors in the rural health. Exhibiting good antimicrobial activity,
area and the change of human eating habits. 2-3 Nigella sativa L. seed, known as black cumin, has
Gram positive bacteria belongs to Streptococcus been widely used as food preservatives. 12-13
genus such as Streptococcus mutans, Streptococcus Antimicrobial activity of N. sativa seed against
salivarius, Streptococcus sanguis and various strains of Streptococcus has also been
Streptococcus sorbinus have been found to play an reported previously. 14-15
important role in human dental decay. 4-7
QUICK RESPONSE CODE Anti-inflammatory, anticancer, antioxidant,
DOI: immunomodulation, antiglycemic and
10.13040/IJPSR.0975-8232.8(7).3155-61
hepatoprotective activities are some biological
activities of N. sativa seed crude extract or essential
Article can be accessed online on: oil that have been scientifically revealed, with
www.ijpsr.com
thymoquinone as the main bioactive constituent.16-
19
DOI link: http://dx.doi.org/10.13040/IJPSR.0975-8232.8 (7).3155-61

International Journal of Pharmaceutical Sciences and Research 3155

Gasong et al., IJPSR, 2017; Vol. 8(7): 3155-3161. E-ISSN: 0975-8232; P-ISSN: 2320-5148

Previously, our study has been successfully Mueller Hinton Agar, thereafter each sterile disk
designed the optimum extraction method of N. was added with 10 μl of DLBS1355 o/w emulsion,
sativa seed oil extract using supercritical fluid and then were placed on agar. All plates were then
extraction using carbon dioxide (SCFE-CO2) and incubated at temperature of 37 °C for 48 h.
investigated its antimicrobial activity. The results Presence of clear zone around the disk was
showed that N. sativa seed oil extract was found to considered as inhibition zone and the diameter was
be more effective to inhibit the growth of Gram measured.
positive pathogenic bacteria. 20 In the present study,
we evaluated the antimicrobial activity of oil-in- Minimum inhibitory concentration (MIC)
water (o/w) emulsion of previously obtained N. determination: The minimum inhibitory
sativa seed oil extract, which was named as concentration (MIC) was determined by broth
DLBS1355, against two most common causative dilution method using a 96-microwell plate. The 24
dental cariogenic bacteria, Streptococcus mutans h culture of each S. mutans and S. sanguis
and Streptococcus sanguis. (approximately 107CFU/ml) were respectively
inoculated into BHIB supplemented with various
MATERIALS AND METHODS: concentrations of DLBS1355 o/w emulsion. MIC
Chemical and culture media: Bacterial strains was determined as the concentration that firstly
were obtained from American Type Culture exhibited a reduction on the visual growth.
Collection (ATCC). All bacterial media and
chemicals were purchased from Merck (Germany) Time kill assay: Time kill assay was assessed in
unless explained elsewhere and Kolliphor HS15 broth medium as described in previous study21
was obtained from Megasetia Agung Kimia with modification. Both S. mutans and S. sanguis
(Indonesia). were inoculated separately on BHIB and incubated
for 5 h to obtain the log-phase culture (107-8
Preparation of DLBS1355 emulsion: DLBS1355 CFU/ml). DLBS1355 o/w emulsion was then added
o/w emulsion was prepared using Kolliphor HS15 into the medium and incubated at temperature of 37
and propylene glycol as surfactant. DLBS1355 o/w °C. The viable cells of S. mutans and S. sanguis
emulsion was made by mixing 1.4 g Kolliphor were enumerated at 0, 15, 30, 75 and 120 min after
HS15 and 0.2 g propylene glycol for 20-30 min treatment.
using magnetic stirrer at 60 °C. Then, 2 g of
DLBS1355 was added and further mixed for 10 Inhibition of biofilm formation: The ability of the
min. Purified water was added to obtain the final emulsion to inhibit the formation of bacterial
volume of 20 ml DLBS1355 o/w emulsion which biofilm was evaluated by method as described
contains 10% (w/v) N. sativa seed oil extract. previously22 with minor modification. The biofilm
formation inhibition assay was performed on 96-
Bacterial strains and culture condition: Two well microplate. S. mutans, S. sanguis and mixed
strains of dental cariogenic bacteria belonging to culture of S. mutans and S. sanguis were
Streptococcus genus were used in this study. respectively inoculated into BHIB that
Streptococcus mutans ATCC 35668 and supplemented by glucose and o/w emulsion
Streptococcus sanguis ATCC 10556 were containing 0.5% N. sativa seed oil extract and
cultivated into brain heart infusion broth (BHIB) at incubated for 72 h. S. mutans and S. sanguis
37 °C for 24 h prior to usage. cultivated into BHIB without emulsion were
determined as negative control. After incubation,
Antimicrobial activity evaluation: Preliminary the planktonic cells were discarded and biofilm
evaluation of antimicrobial activity of DLBS1355 formed on the bottom of the well was washed twice
o/w emulsion was done by disk diffusion method using sterile purified water. The biofilm was
according to the general guide from Clinical and evaluated qualitatively by adding 0.01% crystal
Laboratory Standards Institute (CLSI) (2003). An violet (v/v) for 30 min. The remaining crystal violet
approximately 106 CFU/ml of S. mutans and S. was discarded and washed twice with water.
sanguis culture were respectively spread onto

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Scanning electron microscopy (SEM) analysis: kill assay of DLBS1355 o/w emulsion containing
To investigate the effect of DLBS1355 o/w 0.5% N. sativa seed oil extract exhibited
emulsion on bacterial cellular morphology and bactericidal effect against S. mutans (Fig. 1a) and
growth, visualization using scanning electron S. sanguis (Fig. 1b). After 2 h of administration,
microscope was performed. S. mutans and S. the number of viable cells was reduced
sanguis were respectively cultured into emulsion significantly. The bactericidal effect was found to
supplemented BHIB with 0.5% N. sativa seed oil be more effective against S. sanguis compared to S.
extract as the final concentration. After incubation, mutans. Significant reductions on the number of
cells were separated from media by centrifugation viable cells were observed during the first 15 min
and washed twice using sterile phosphate-buffered for S. sanguis, and 75 min for S. mutans.
saline (PBS). A solution of 10% formaldehyde in
PBS was used for fixation followed by gradual
dehydration using increased concentration of
ethanol. The dehydrated cells were air-dried and
then coated with gold for further visualization
using JEOL JSM 6510 scanning electron
microscope.

RESULTS:
Antimicrobial evaluation: Disk diffusion assay
was used in preliminary investigation of the
antimicrobial activity of DLBS1355 o/w emulsion a
against S. mutans and S. sanguis. Optimization
inhibition activity of the N. sativa seed oil extract
against some Gram positive pathogenic bacteria
was done in previous study. 20 Concentration of N.
sativa seed oil extract used in optimization of
inhibition activity in previous study was 3-10% of
final concentration. Therefore, DLBS1355 o/w
emulsion containing 10% N. sativa seed oil extract
was used in this study. A marked inhibition zone
was found in this study indicating a strong growth b
inhibition activity of DLBS1355 o/w emulsion FIG. 1: TIME KILL ASSAY OF DLBS1355 O/W
against S. mutans and S. sanguis (Table 1). EMULSION CONTAINING 0.5% N. SATIVA OIL
EXTRACT AGAINST (a) S. MUTANS AND (b) S.
Emulsion without N. sativa seed oil extract did not SANGUIS
inhibit S. mutans and S. sanguis growth (data not
shown). The inhibition activity of DLBS1355 o/w Biofilm formation inhibition assay: The effect of
emulsion shown in this study was similar to that DLBS1355 o/w emulsion on biofilm formation was
obtained in our previous study.20 evaluated qualitatively using crystal violet staining.
Compared to negative control, which was the
TABLE 1: ANTIBACTERIAL ACTIVITY EVALUATION OF untreated biofilm, the effect of DLBS1355 o/w
DLBS1355 O/W EMULSION
emulsion containing 0.5% N. sativa seed oil extract
Bacteria Diameter of IZ (mm) * MIC (%) **
S. mutans 32.75 ± 8.38 0.110 was clearly seen on the inhibition of biofilm
S. sanguis 52.00 ± 1.92 0.037 formation of both S. mutans and S. sanguis (Fig. 2).
IZ: Inhibition zone; MIC: Minimum inhibitory concentration Similar to that shown on planktonic cells, the
*Conducted using DLBS1355 o/w emulsion containing 10% emulsion showed a more effective inhibition on the
N. sativa seed oil extract biofilm formation of S. sanguis compared to S.
** Concentration of N. sativa seed oil extract in emulsion
mutans, as shown by diameters of inhibition zone
(Table 1).
Time kill assay: Time kill assay was performed at
a 5-fold concentration of the highest MIC. Time

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The completely inhibited biofilm formation of S. the higher antibacterial activity of N. sativa seed
sanguis indicates a significant reduction of the extract and oil extract on Gram positive bacteria. 20,
23-27
viable cells caused by DLBS1355 o/w emulsion. Furthermore, the antibacterial activity of N.
sativa seed extract and its constituents against some
strains of Streptococcus associated with dental
caries has been reported as well.14, 28 Consistent to
the results of previous studies, the present study
demonstrated a strong growth inhibition and
bactericidal activity of DLBS1355 o/w emulsion
against S. mutans and S. sanguis, with a slightly
higher activity on S. sanguis.
The strong antibacterial activity showed in this
FIG. 2: BIOFILM FORMATION INHIBITION
study further indicated that emulsification process
ABILITY OF DLBS1355 O/W EMULSION did not significantly affect antibacterial activity of
VISUALIZED USING CRYSTAL VIOLET N. sativa seed oil extract showed in previous study.
As one of widely used lipophilic compound
delivery systems, oil emulsification is able to
enhance their solubility in aqueous-based system,
increase the compound stability and somehow
improve the biological activity. 29-33 One important
virulence factor of oral Streptococci is its biofilm
formation ability during its attachment on solid
surfaces. The bacterial biofilms are more difficult
to remove compared to planktonic bacterial cells.
34-35
Therefore, the evaluation of biofilm formation
inhibition activity was also conducted in this study.
DLBS1355 o/w emulsion, which contains 0.5% N.
sativa seed oil extract, effectively inhibited biofilm
FIG. 3: EFFECT OF DLBS1355 O/W EMULSION ON S. formation of S. mutans, S. sanguis and mixed
MUTANS (a, c) AND S. SANGUIS (b, d) CELLULAR culture of S. mutans and S. sanguis.
MORPHOLOGY VISUALIZED USING SEM
The inhibition effect of N. sativa seed oil extract on
Scanning electron microscopy (SEM) analysis: biofilm formation of Gram positive bacteria was
The effect of DLBS1355 o/w emulsion on the also reported previously with a concentration-
cellular morphology of S. mutans and S. sanguis dependent manner. 24 The fundamental enzymes
was examined using scanning electron microscope involved on Streptococcus biofilm formation,
as shown in Fig. 3. After the growth of bacteria in glucosyltransferase and fructosyltransferase, were
DLBS1355 o/w emulsion-supplemented BHIB for reported to be inhibited by synthetic antimicrobial
18 h, significant morphology alteration was found agents and several essential oils of medicinal
on S. mutans and S. sanguis (Fig. 3c-d). Cellular plants, including N. sativa. 36-40 Those compounds
damages were clearly seen on the bacterial surface. were also able to inhibit the adhesion of the
The cell wall and cytoplasmic membrane disruption Streptococcus cells and further affected the biofilm
that were possibly caused by the emulsion activity oxidative activity. 24, 41
allowed the cytoplasm and cellular constituents to
be discharged from the cell. Inhibition effect on bacterial growth together with
cell adhesion and physiological activity leads to the
DISCUSSION: Broad spectrum antimicrobial inhibition of biofilm formation. Antagonism effects
activity of N. sativa L. seed has been well- on biofilm formation were commonly found on
documented previously. However, our previous some strains of Streptococcus genus.
study and other studies have been highlighted on

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Gasong et al., IJPSR, 2017; Vol. 8(7): 3155-3161. E-ISSN: 0975-8232; P-ISSN: 2320-5148

A study mentioned that the formation of S. mutans CONCLUSION: Based on the result of the present
biofilm was suppressed by the presence of S. study, it can be concluded that N. sativa oil extract
oligofermentans. 42 In this study, the biofilm (DLBS1355) formulated in oil in water (o/w)
formed by S. mutans cultured together with S. emulsion possesses antimicrobial activity against
sanguis was slightly inhibited compared to the dental cariogenic bacteria. It further showed the
biofilm from single culture of S. mutans (Fig. 2), potential use of DLBS1355 o/w emulsion to
which was similar to the result of the previous prevent and/or cure the common oral diseases.
study. The most suggested bacteriostatic and Further study is needed to investigate its
bactericidal mechanisms of natural antimicrobial cytotoxicity regarding to human use.
agents including N. sativa are related to the
integrity and function of the cell wall and ACKNOWLEDGEMENT: The author would like
cytoplasmic membrane. Peptidoglycan layer to thank to Edward Widjojokusumo for providing
damage and cell wall leakage caused by several the emulsion, and Siswa Setyahadi and Isabela
medicinal plants active compounds leading to Anjani for critical review on this manuscript.
morphological changes on gram positive
CONFLICT OF INTEREST: The authors
pathogenic bacteria were reported previously. 43-44
declared no conflict of interest with respect to
In this study, we also observed the significant authorship and/or publication.
morphological alteration on the cell growth of S.
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How to cite this article:

Gasong BT, Hartanti AW and Tjandrawinata RR: Antibacterial activity of Nigella sativa L Seed oil in water emulsion against dental
cariogenic bacteria. Int J Pharm Sci Res 2017; 8(7): 3155-61.doi: 10.13040/IJPSR.0975-8232.8(7).3155-61.

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