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367
ABSTRACT
Context: Glass ionomer cement (GIC) is known for its
antimicrobial activity due to its low pH and uoride
release. The uoride released has an inhibitory
effect on a nite number of bacteria which leads
to the risk of recurrent caries. Additives such as
chlorhexidine (CHX) and triclosan have been tried to
maximize the antibacterial activity of GIC. Although
CHX is known for its impressive antimicrobial action,
it has adverse after effects which include alteration of
commensal oral ora, staining of teeth, etc., Hence, there
is a need for a material with improved antimicrobial
efcacy with nominal side effects. Aim: The aim of
this study is to assess the antimicrobial efcacy of
conventional GIC added with Propolis, Chitosan (CH),
and CHX against Streptococcus mutans and Lactobacillus
acidophilus. Materials and Methods: Eighty discs of
size 10 × 2 mm are prepared with Conventional GIC
and GIC added with Propolis, CH and CHX (n = 10)
and tested against S. mutans and L. acidophilus using the
agar diffusion assay. Zones of inhibition are measured
for day 1, 7, and 14, and the data were tabulated and
analyzed. Statistical Analysis: One‑way ANOVA test
for intragroup and Tukey’s post hoc test for intergroup
comparison. Results: The mean value of zone of
inhibition (in mm) against S. mutans on day 14 for Group
I, II, III, and IV are 11.70 ± 1.49, 16.50 ± 2.23, 19.30 ± 2.87,
and 15.60 ± 2.76, respectively. For L. acidophilus, the
mean value of the zone of inhibition (in mm) on day 14
are 8.40 ± 0.97, 9.70 ± 0.68, 16.20 ± 2.04, and 12.50 ± 0.97
for Group I, II, III, and IV, respectively. Conclusion:
Higher antimicrobial activity was shown by GIC with
CHX against both strains. GIC with Propolis and GIC
with CH were effective in inhibiting S. mutans and
L. acidophilus, respectively.
KEYWORDS: Antimicrobial activity, chitosan,
chlorhexidine, glass ionomer cement, propolis
Comparative evaluation of antimicrobial efcacy of
glass ionomer cement added with propolis, chitosan,
and chlorhexidine against Streptococcus mutans and
Lactobacillus acidophilus: An in vitro study
B.Neelima1, J. Sharada Reddy2, P. Tara Singh3, K.Suhasini3, I.Hemachandrika3, Shaik Hasanuddin3
1Senior Resident, 2Professor and Head, 3Associate Professor, Department of Pedodontics and Preventive Dentistry, Government Dental
College and Hospital, Hyderabad,Telangana State, India
Introduction
Glass ionomer cement (GIC) is a successfully used
restorative material in the clinical practice having favorable
features such as chemical bonding to the tooth, uoride
release, and biocompatibility. It exerts an antimicrobial
effect due to its low pH and uoride release.[1] The effect
of uoride lasts for a brief duration, and it acts on a limited
Address for correspondence:
Dr. J.Sharada Reddy, MDS, Professor and Head, Department of
Pedodontics and Preventive Dentistry, Room No 305, 2nd Floor,
Government Dental College and Hospital, Afzalgunj, Hyderabad,
500 012; Telangana State, India.
E‑mail: sharadagdchyd@gmail.com
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DOI:
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How to cite this article: Neelima B, Reddy JS, Singh PT,
Suhasini K, Hemachandrika I, Hasanuddin S. Comparative
evaluation of antimicrobial efficacy of glass ionomer cement
added with propolis, chitosan, and chlorhexidine against
Streptococcus mutans and Lactobacillus acidophilus: An in vitro
study. J Indian Soc Pedod Prev Dent 2020;38:367-73.
Submitted: 17-Jul-2020 Revised: 03-Sep-2020
Accepted: 08-Sep-2020 Published: 05-Jan-2021
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Original Article
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Neelima, et al.: Antimicrobial ecacy of modied GIC against S. mutans and L. acidophilus
Journal of Indian Society of Pedodontics and Preventive Dentistry | Volume 38 | Issue 4 | October-December 2020 |
368
spectrum of bacteria. Owing to these limitations, additives
are added to augment the antibacterial property.
Chlorhexidine (CHX), a bisbiguanide, is a potent
antimicrobial agent. It has been proven as an effective
anti‑plaque agent. Its antimicrobial effect lasts long
due to its prolonged retention in oral tissues.[2,3]
Chitosan (CH) is a deacetylated derivative from
bio‑polysaccharide chitin. It is a weak base that is
insoluble in water but soluble in dilute aqueous acid
solution such as acetic acid. Its diverse antimicrobial
activity is seen against lamentous fungi, yeasts,
and bacteria. It is more active against Gram‑positive
bacteria than Gram‑negative bacteria.[4‑6]
Propolis is a natural derivative, retrieved from the
beehive. It exerts numerous biological activities such as
antibacterial, antifungal, antiviral, anti‑inammatory,
bio‑stimulative properties attributed to compounds such
as polyphenols, aromatic acids, and diterpenic acids. The
antibacterial activity is primarily ascribed to avonoids.[7,8]
As there has been limited literature which comparatively
evaluated the antimicrobial properties of the above
said three materials, a study was planned to assess the
antimicrobial efcacy of conventional GIC added with
Propolis, CHX, and CH against Streptococcus mutans
and Lactobacillus acidophilus, which are known to be the
main etiological agents in dental caries initiation and
progression.
Materials and Methods
The present study consisted of four groups for each
strain to be tested, namely S. mutans (MTCC 497) and
L. acidophilus (MTCC 10307) (Institute of Microbial
Technology, Chandigarh, India). Each group comprised
of 10 specimens to achieve 80% power to detect the
differences among the means at 0.05% signicance
level. The groups are: Group I: Conventional GIC, Fuji
IX (GC Corporation, Tokyo, Japan); Group II: GIC with
Propolis (HiTech Natural Products Ltd., New Delhi,
India); Group III: GIC with CHX (Basic Pharma Life
Sciences Pvt. Ltd, Ankleshwar, Gujarat, India); and
Group IV: GIC with CH(In Life Pharma Pvt. Ltd.,
Hyderabad, India).
Preparation of propolis modied glass ionomer
cement
Ethanol soluble liquid Propolis (ESLP) was diluted
from 86% to obtain a nal concentration of 25%. Ratio
used for specimens preparation‑powdered GIC: Liquid
GIC: ESLP = 1: 0.75: 0.25. ESLP was added after mixing
powder and liquid of GIC.
Preparation of chlorhexidine modied glass
ionomer cement
CHX base (0.2 g) was added to 20 ml of acetic acid
to obtain a 1% solution of CHX diacetate. From 1%
solution of CHX diacetate, 0.07 ml of liquid was
mixed with 6.4 ml of GIC liquid. The powder/liquid
ratio recommended for restorative purposes by the
manufacturer was adopted, i.e., one scoop of powder
to one drop of liquid.
Preparation of chitosan modied glass ionomer
cement
Twenty milligrams of CH was weighed and dissolved
in 0.3 N acetic acid and made up to 100 ml with the
same acetic acid in a 100 ml standard ask to get
0.2 mg/ml. Then 0.1 ml of 0.2 mg/ml of CH solution
was added to 0.9 ml of GIC liquid to get 10% v/v CH
modied glass ionomer solution.
Specimen preparation
Total eighty discs were prepared for four groups using
a circular brass mold of dimensions 10 mm × 2 mm.
Assessment of antimicrobial property
The bacterial strain from stock cultures were cultivated
in specic culture broths, i.e., brain heart infusion (BHI)
broth for the growth of S. mutans and De Man Rogosa
Sharpe (MRS) broth for L. acidophilus for 24 h and
48 h, respectively. The cultures were then diluted with
their respective broths to obtain turbidity equal to
1.5 × 108 CFU/ml equivalent to 0.5 McFarland turbidity
which was conrmed with Spectrophotometer by
measuring the absorbance at a wavelength of 600 nm.
Twenty Petri dishes (9 cm diameter) containing 10 ml
agar to a thickness of 2 mm were prepared. BHI Agar
was used for S. mutans and MRS Agar was used for
L. acidophilus. Using a sterile swab, the entire surface of
the agar plate was swabbed to ensure even distribution
of the inoculums. For each Petri dish, four standardized
wells with a diameter of 10 mm were punched into the
agar with the agar puncher, and four specimens one
from each group were inserted into the wells with
sterile forceps. They were incubated at 37°C ± 1°C
for 24 h for S. mutans and 48 h for L. acidophilus. The
diameter of the inhibition zones produced around
the specimens (specimens + inhibition zones) was
measured in millimeters with a digital caliper at three
different points, and the mean was recorded as the
day 1 value. The bacterial population usually dies
due to the release of toxic metabolites if cultures are
kept for a long duration. Hence, on day 7 and 14, fresh
agar plates were used and cultured, and the specimens
were transferred, and incubated and inhibition zones
were calculated.
Results
The data were analyzed using the one‑way ANOVA
test for intragroup comparison, whereas intergroup
comparison was done by Tukey’s post hoc test (SPSS
version 20). The mean values of zones of inhibition for
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Neelima, et al.: Antimicrobial ecacy of modied GIC against S. mutans and L. acidophilus
Journal of Indian Society of Pedodontics and Preventive Dentistry | Volume 38 | Issue 4 | October-December 2020 | 369
Group I, II, III, and IV were 13.90 ± 2.38, 19.70 ± 2.63,
23.00 ± 3.43 , and 19.50 ± 2.68 (in mm) on day 1
and on day 14; they were 11.70 ± 1.49, 16.50 ± 2.23,
19.30 ± 2.87, and 15.60 ± 2.76 (in mm), respectively,
for S. mutans [Table 1]. For L. acidophilus, the mean
values were 12.40 ± 0.97, 13.70 ± 0.68, 20.30 ± 2.00,
and 16.50 ± 0.97 (in mm), on day 1 and 8.40 ± 0.97,
9.70 ± 0.68, 16.20 ± 2.04, and 12.50 ± 0.97 (in mm) on
day 14, respectively, [Table 2].
The intergroup comparison of four groups against
S. mutans showed higher mean values of the zone of
inhibition for Group III (GIC with CHX) followed by
Group II (GIC with Propolis), Group IV (GIC with CH),
and Group I (Conventional GIC, Fuji IX). The difference
was statistically signicant at a probability level
of <0.001 on day 1, day 7, and day 14 [Tables 3‑5],
respectively.
For L. acidophilus, the inhibition zones were higher for
Group III followed by Group IV, Group II, and Group
I which was statistically signicant (P < 0.001) on day
1, day 7, and day 14 [Tables 6‑8], respectively.
Discussion
GIC is the most widely used restorative material
because of its favorable characteristics such as its
adhesive effect and uoride release. However, the
uoride released is not adequate to alter the growth
of bacteria and inhibit them. This leads to the risk
of recurrent caries around the GIC restorations. To
overcome this problem, the addition of antibacterial
agents can be a therapeutical advantage.
Agar plate diffusion was employed in this study
because set materials can be assayed through this
procedure. It is a widely accepted simple screening
assay to assess the antibacterial properties of
restorative materials. Moreover, its simplicity, ability
to test many specimens, and relatively low cost are the
other advantages of this assay.
All the four groups of restorative materials in
the present study showed antimicrobial activity
against S. mutans and L. acidophilus on day 1, 7, and
14 (P < 0.001). The antimicrobial activity exhibited by
GIC with CHX was the highest, and Conventional GIC
was the least. Propolis exhibited higher antimicrobial
activity against S. mutans than with L. acidophilus. CH
exhibited signicant antimicrobial activity against
L. acidophilus than with S. mutans.
The mean zone of inhibition of GIC with
CHX (Group III) was more against S. mutans than
compared to Lactobacillus. The values reported in this
study were a little higher in contrast to those obtained
by Mittal et al., Türkün et al., and Takahashi et al.[2,9,10]
This difference could be attributed to the liquid form of
CHX diacetate, which was used in the present study.
Liquid can diffuse well into the agar and exhibit more
antibacterial action. The decline in antibacterial activity
from day 1 to day 7 and day 14 could be attributed to
the concomitant decline in the available concentration
of CHX with time. The decrease in CHX may be a result
of the loss of material by elution or the decrease in
CHX is related to the formation of insoluble salts with
GIC. Although the concentration of CHX is decreased
with time, the level of CHX in the micro‑environment
might be sufcient to prevent secondary caries for
an extended period of time. It was suggested that a
decrease in CHX concentration with time leads to the
recolonization of less‑sensitive microorganisms on
the tooth and prevent S. mutans from re‑establishing
on the tooth surface.[11] The concentration used (1%)
was optimal to provide antibacterial activities without
altering the mechanical properties, bonding abilities,
or setting time of GIC. CHX diacetate is preferable to
use over CHX digluconate as it is a stable material and
is not prone to decomposition.
The mean zone of inhibition in Group II (GIC with
Propolis) was signicant against S. mutans and
L. acidophilus (P < 0.001). The activity of propolis against
microorganisms was more related to the synergistic
effects of avonoids than individual compounds. The
components of propolis extract such as avonoids,
caffeic acid, and cinnamic acid inuence the microbial
membrane or cell wall sites, resulting in functional
and structural defects. The presence of propolis in
the matrix of glass ionomer creates a pathway for the
release of uoride ions which confers an additional
advantage to the restorative materials. The mean values
obtained in the present study were 19.70 ± 2.67 mm
against S. mutans which was higher to that obtained by
Airen et al.[12] where they used 20% Ethanolic Extract
of Propolis (EEP), which exhibited a mean diameter
of 12.4 ± 1.46 mm against S. mutans. The higher values
Table 1: Mean values of zones of inhibition
(in mm) of four groups on day 1, 7 and 14 against
Streptococcus mutans
Groups Day 1 Day 7 Day 14
Conventional GIC 13.90±2.38 12.60±2.12 11.70±1.45
GIC with propolis 19.70±2.67 18.50±2.51 16.50±2.22
GIC with chlorhexidine 23.00±3.43 20.00±3.13 19.30±2.87
GIC with chitosan 19.50±2.68 17.60±2.76 15.60±2.76
GIC=Glass ionomer cement
Table 2: Mean values of zones of inhibition
(in mm) of four groups on day 1, 7 and 14 against
Lactobacillus acidophilus
Groups Day 1 Day 7 Day 14
Conventional GIC 12.40±0.97 10.30±0.94 8.40±0.97
GIC with propolis 13.70±0.68 11.70±0.68 9.70±0.68
GIC with chlorhexidine 20.30±2.00 18.30±2.00 16.20±2.04
GIC with chitosan 16.50±0.98 14.50±0.98 12.50±0.98
GIC=Glass ionomer cement
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Neelima, et al.: Antimicrobial ecacy of modied GIC against S. mutans and L. acidophilus
Journal of Indian Society of Pedodontics and Preventive Dentistry | Volume 38 | Issue 4 | October-December 2020 |
370
obtained in our study could be due to the difference
in the concentration used (25%) or may be due to the
combined antibacterial effect of GIC and Propolis. The
effect of concentration on antimicrobial activity is yet
to be concluded since the studies so far done are few
and they are contradictory to each other. According to
Topcuoglu et al.,[13] the diameters of zones of inhibition
determined against S. mutans were not based upon the
concentration of EEP. Hatunoğlu et al.[14] found that
25% and 50% EEP added to GIC inhibited S. mutans
but inhibition was not seen with 10% EEP. In the
well‑diffusion test conducted by Elgamily et al.,[15] the
diameter of inhibitory zones was 32.60 ± 2.22 mm with
1.25% Propolis added to GIC, and they concluded
that the results were concentration dependent. The
difference in the values of various studies could be
attributed to the geographical origin of propolis,
variations in the strains used, and the type of agar used.
Table 3: Intergroup comparison of the four groups on day 1 against Streptococcus mutans
Streptococcus mutans Groups (I) Mean values of zones of inhibition (in mm) Groups (J) Mean difference (I-J) P
Day 1 Conventional
GIC
13.90 Propolis −5.800* 0.0001
Chlorhex −9.100* 0.0001
Chitosan −5.600* 0.0001
GIC with
propolis
19.70 GIC 5.800* 0.0001
Chlorhex −3.300 0.058
Chitosan 0.200 0.999
GIC with
chlorhexidine
23.00 GIC 9.100* 0.0001
Propolis 3.300 0.058
Chitosan 3.500* 0.040
GIC with
chitosan
19.50 GIC 5.600* 0.0001
Propolis −0.200 0.999
Chlorhex −3.500* 0.040
*Signicant. P=Probability; GIC=Glass ionomer cement
Table 5: Inter group comparison of four groups on day 14 against Streptococcus mutans
Streptococcus mutans Groups (I) Mean values of zones of inhibition (in mm) Groups (J) Mean difference (I-J) P
Day 14 Conventional
GIC
11.70 Propolis −4.800* 0.000
Chlorhex −7.600* 0.000
Chitosan −3.900* 0.005
GIC with
propolis
16.50 GIC 4.800* 0.000
Chlorhex −2.800 0.060
Chitosan 0.900 0.836
GIC with
chlorhexidine
19.30 GIC 7.600* 0.000
Propolis 2.800 0.060
Chitosan 3.700* 0.008
GIC with
chitosan
15.60 GIC 3.900* 0.005
Propolis −0.900* 0.836
Chlorhex −3.700* 0.008
*Signicant. P=Probability; GIC=Glass ionomer cement
Table 4: Intergroup comparison of the four groups on day 7 against Streptococcus mutans
Streptococcus mutans Groups (I) Mean values of zones of inhibition (in mm) Groups (J) Mean difference (I-J) P
Day 7 Conventional
GIC
12.60 Propolis −5.900* 0.0001
Chlorhex −7.400* 0.0001
Chitosan −5.000* 0.001
GIC with
Propolis
18.50 GIC 5.900* 0.0001
Chlorhex −1.500 0.594
Chitosan 0.900 0.874
GIC with
Chlorhexidine
20.00 GIC 7.400* 0.0001
Propolis 1.500 0.594
Chitosan 2.400 0.201
GIC with
Chitosan
17.60 GIC 5.000* 0.001
Propolis −0.900 0.874
Chlorhex −2.400 0.201
*Signicant. P=Probability; GIC=Glass ionomer cement
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Neelima, et al.: Antimicrobial ecacy of modied GIC against S. mutans and L. acidophilus
Journal of Indian Society of Pedodontics and Preventive Dentistry | Volume 38 | Issue 4 | October-December 2020 | 371
Against L. acidophilus the inhibition zones shown by
Group II (GIC with Propolis) when compared to Group
III (GIC with CHX) and Group IV (GIC with CH)
were smaller but were signicantly larger (P < 0.001)
when compared to Group I (Conventional GIC). This
indicates that GIC with propolis was effective against
L. acidophilus up to some extent but not as effective as
that of GIC with CH and GIC with CHX. These results
were closer to that of a study done by Airen et al.[12]
These features exhibited by propolis and CH promises
a new ray of hope for their use as an additive into
restorative materials as they are effective not only on
S. mutans but also on L. acidophilus.
The mean zone of inhibition shown by
Group IV (GIC with CH) was smaller when compared
to the other two groups, namely Group II (GIC with
Propolis) and Group III (GIC with CHX) but larger
Table 8: Inter group comparison of four groups on day 14 against Lactobacillus acidophilus
Lactobacillus acidophilus Groups (I) Mean values of zones of inhibition (in mm) Groups (J) Mean difference (I-J) P
Day 14 GIC 8.40 Propolis −1.300 0.122
Chlorhex −7.800* 0.0001
Chitosan −4.100* 0.0001
GIC with
propolis
9.70 GIC 1.300 0.122
Chlorhex −6.500* 0.0001
Chitosan −2.800* 0.0001
GIC with
chlorhexidine
16.20 GIC 7.800* 0.0001
Propolis 6.500* 0.0001
Chitosan 3.700* 0.0001
GIC with
chitosan
12.50 GIC 4.100 0.0001
Propolis 2.800* 0.0001
Chlorhex −3.700* 0.0001
*Signicant. P=Probability; GIC=Glass ionomer cement
Table 6: Inter group comparison of four groups on day 1 against Lactobacillus acidophilus
Lactobacillus acidophilus Groups (I) Mean values of zones of inhibition (in mm) Groups (J) Mean difference (I-J) P
Day 1 GIC 12.40 Propolis −1.300 0.115
Chlorhex −7.900* 0.0001
Chitosan −4.100* 0.0001
GIC with
propolis
13.70 GIC 1.300 0.115
Chlorhex −6.600* 0.0001
Chitosan −2.800* 0.0001
GIC with
chlorhexidine
20.30 GIC 7.900* 0.0001
Propolis 6.600* 0.0001
Chitosan 3.800* 0.0001
GIC with
chitosan
16.50 GIC 4.100* 0.0001
Propolis 2.800* 0.0001
Chlorhex −3.800* 0.0001
*Signicant. P=Probability; GIC=Glass ionomer cement
Table 7: Inter group comparison of four groups on day 7 against Lactobacillus acidophilus
Lactobacillus acidophilus Groups (I) Mean values of zones of inhibition (in mm) Groups (J) Mean difference (I-J) P
Day 7 GIC 10.30 Propolis −1.400 0.078
Chlorhex −8.000* 0.0001
Chitosan 4.200* 0.0001
GIC with
propolis
11.70 GIC 1.400 0.078
Chlorhex −6.600* 0.0001
Chitosan 2.800* 0.0001
GIC with
chlorhexidine
18.30 GIC 8.000* 0.0001
Propolis 6.600* 0.0001
Chitosan 3.800* 0.0001
GIC with
chitosan
14.50 GIC 4.200* 0.0001
Propolis 2.800* 0.0001
Chlorhex 3.800* 0.0001
*Signicant. P=Probability; GIC=Glass ionomer cement
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Neelima, et al.: Antimicrobial ecacy of modied GIC against S. mutans and L. acidophilus
Journal of Indian Society of Pedodontics and Preventive Dentistry | Volume 38 | Issue 4 | October-December 2020 |
372
when compared to Group I (Conventional GIC)
against S. mutans [Figure 1]. Higher values were seen
in our study in contrast to that of Mishra et al.[1] and
Ahmed et al.[16] This difference could be possibly due
to the variation in the method of measurement of the
inhibition zone. Debnath et al.[4] found that modication
of conventional GIC with 10% v/v CH improved the
antibacterial property of GIC against S. mutans. CH
exerts antimicrobial activity by modifying the electric
potential of the cell wall of bacteria and also its acidic
nature which prevents the microbial growth and by
promoting the release of uoride.
Against L. acidophilus, the zone of inhibition shown
by GIC with CH was larger compared to GIC with
Propolis and Conventional GIC but smaller when
compared to GIC with CHX [Figure 2]. This suggests
that GIC with CH is more effective than GIC with
propolis and conventional GIC, but it is not as effective
as with CHX against L. acidophilus.
Limitations of the study
In the present in vitro study, the antimicrobial efcacy
of the study materials was tested against standard
strains. However, the antibacterial effect of these
restorative materials in the oral cavity may vary
because of the multitude of microorganisms present
in oral biolm. Hence, further clinical studies should
be undertaken to compare these study materials with
different concentrations to explore their antimicrobial
activity against diverse oral microora.
Conclusion
All the four groups of restorative materials exhibited
antibacterial activity from day 1 to day 14 among which
CHX had shown signicantly larger zones of inhibition
against S. mutans and L. acidophilus. All the groups had
shown higher antimicrobial activity against S. mutans
than L. acidophilus.
Although CHX showed a large zone of inhibition against
both the strains used in the study, it could adversely
affect the commensal microora and is harmful to
pulpal cells when placed in deep cavities. The two
natural substances used in the study, i.e., Propolis and
CH were effective against S. mutans and L. acidophilus.
With the current trend, “shift to nature,” these natural
derivatives which also have an added advantage of
uoride release can have a novel and promising role
in treating dental caries. This is especially useful in
children affected with early childhood caries and also
in those exhibiting behavioral problems in whom
cavity cutting and restoration could be challenging.
Financial support and sponsorship
Nil.
Conicts of interest
There are no conicts of interest.
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Figure 1: Antimicrobial efcacy of four groups against Streptococcus
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Journal of Indian Society of Pedodontics and Preventive Dentistry | Volume 38 | Issue 4 | October-December 2020 | 373
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