UNIVERSIDADE ESTADUAL PAULISTA
“JÚLIO DE MESQUITA FILHO”
Instituto de Ciência e Tecnologia
Campus de São José dos Campos
ORIGINAL ARTICLE DOI: https://doi.org/10.4322/bds.2023.e3440
1
Braz Dent Sci 2023 Apr/Jun;26 (2): e3440
Analysis of biofilm formation by
Candida albicans
in different types
of orthodontic fixed appliances and devices
Análise da formação de biofilme por
Candida albicans
em diferentes tipos de aparelhos e dispositivos ortodônticos fixos
Ellen Eduarda FERNANDES
1
, Daniela Fernandes Lobo Molica OLIVEIRA
1
, Renata Pilli JÓIAS
1
, Pamela Aparecida DINIZ
1
,
Patrícia Pimentel de BARROS
2
, Antônio Olavo Cardoso JORGE
1
, Wagner de OLIVEIRA
3
, Sigmar de Mello RODE
3
1 - Universidade Estadual Paulista “Júlio de Mesquita Filho”, Instituto de Ciência e Tecnologia, Departamento de Biociências e
Diagnóstico Bucal, São José dos Campos, SP, Brazil.
2- Escola Multicampi de Ciências Médicas, Universidade Federal do Rio Grande do Norte (UFRN), Caicó, RN, Brazil.
3 - Universidade Estadual Paulista “Júlio de Mesquita Filho”, Instituto de Ciência e Tecnologia, Departamento de Materiais Odontológicos
e Prótese, São José dos Campos, SP, Brasil.
How to cite: Fernandes EE, Oliveira DFLM, Jóias RP, Diniz PA, Barros PP, Jorge AOC, et al. Analysis of biolm formation by
Candida albicans
in different types of orthodontic xed appliances and devices. Braz Dent Sci. 2023;26(2):e3440. https://doi.org/10.4322/bds.2023.e3440
ABSTRACT
Objective: in this study, biolm formation by
Candida albicans
in xed orthodontic appliances was evaluated.
Material and Methods: a total of 300 conventional metal brackets (MC), ceramic (CB), self-ligation (SLB),
nickel-titanium (NiTi), and nickel-chromium (NiCr) wires, and ligatures types were organized into thirty groups
(n=10). To induce biolm formation, brackets, wires, and ligatures were joined, sterilized, placed in 24-well
plates, contaminated with standardized suspensions of
C. albicans
(10
7
cells/mL), and incubated at 37 °C for
48 h with shaking. The biolms formed were detached using an ultrasonic homogenizer, and suspensions were
serially diluted and plated on Sabouraud dextrose agar to determine colony-forming units per mL. Scanning
electron microscopy was performed before and after the biolm formation. Results: lower amount of biolm
formation was observed in the MC group than in the CB and SLB groups (
p
<0.0001). SLB and CB showed similar
biolm formation rates (
p
=0.855). In general, the cross-sectional wires .018”x.025” showed higher biolm
formation when associated with the three types of brackets. When brackets, wires, and ligatures were associated,
the sets with NiCr wires and SSL ligatures with MC brackets (
p
=0.0008) and CB (
p
=0.0003) showed higher
biolm formation. Conclusion: thus, brackets of MC with NiTi and NiCr wires showed lower biolm formation,
regardless of the ligature and cross-sectional or gauge of the wire and, MC and CB brackets with NiCr wires and
SSL ligatures were more likely to accumulate biolms.
KEYWORDS
Biolms,
Candida albicans
, Orthodontic appliances, Orthodontic brackets, Scanning electron microscopy.
RESUMO
Objetivo: neste estudo, a formação de biolme por
Candida albicans
em aparelhos ortodônticos xos foi avaliada.
Material e Métodos: um total de 300 bráquetes metálicos convencionais (MC), cerâmicos (CB), autoligados
(SLB), com os de níquel-titânio (NiTi) e níquel-cromo (NiCr) e tipos de ligaduras foram organizados em
trinta grupos (n=10). Bráquetes, os e ligaduras foram unidos, esterilizados, colocados em placas de 24 poços,
contaminados com suspensões padronizadas de
C. albicans
(10
7
células/mL) e incubados a 37°C por 48 h para
a formação de biolmes. Os biolmes formados foram rompidos por meio de um homogeneizador ultrassônico
e suspensões foram diluídas e semeadas em ágar Sabouraud-dextrose para determinar as unidades formadoras
de colônias por mL. A microscopia eletrônica de varredura foi realizada antes e após a formação do biolme.
Resultados: foi observada menor formação de biolme no grupo MC em comparação aos grupos CB e SLB
(
p
<0,0001). A formação de biolme foi semelhante nos grupos SLB e CB (
p
=0,855). Em geral, os os de seção
2
Braz Dent Sci 2023 Apr/Jun;26 (2): e3440
Fernandes EE et al.
Analysis of biofilm formation by Candida albicans in different types of orthodontic fixed appliances and devices
Fernandes EE et al.
Analysis of biofilm formation by Candida albicans in different
types of orthodontic fixed appliances and devices
INTRODUCTION
Studies have shown that xed orthodontic
appliances are biofilm retainers that can
hinder hygiene [1,2,3], forming sites for
accumulation of food residues and aggregation
of microorganisms [4]. Together, brackets,
wires, bands, and ligatures can further aggravate
these conditions [5]. Although modications in
these accessories are made to minimize biolm
retention, doubts remain regarding whether
these modications result in the greater or lesser
accumulation of residues and microorganisms
when compared with conventional and self-
connected devices [6-10].
The permanent consolidation of biolm can
cause periodontal changes, white spots in the enamel,
and even dental caries [5,11,12]. Many studies have
reported that the main microorganisms involved in
caries are
Streptococcus
spp. and
Lactobacillus
spp
.
However, it is known that caries are not caused by a
limited number of specic bacteria, but by a change
in the microbial population in which
Candida
spp.
play an important role [12].
Candida
is a collecting
agent present in the oral cavity of approximately
30% to 35% of the adult population without
evidence of infection [13]. Therefore, in certain
individuals and in specific situations, they can
assume lamentary form, producing oral diseases
such as oral candidosis.
There is an indication of the cariogenic
potential of
C. albicans
in enamel and dentin lesions
in cooperation with
Streptococcus mutans
[14].
It was observed that glucans produced by certain
bacteria, such as
S. mutans
, can increase the
adhesive capacity of
C. albicans
[15] and that
yeast can be used by
S. mutans
to support its
adhesion and aid the cariogenic process [16].
In vitro
studies suggest
C. albicans
has a high
acidogenic potential and ability to cause mineral
loss and, therefore, is adjunct to the process
of establishment of dental caries [17,18].
In addition, it can increase the incidence of caries
in rats when associated with microbiota with low
cariogenic potential [19].
Perkowski et al. (2019) [20] evaluated oral
microbiota as a risk factor for health complications
in patients treated with removable or xed devices
compared with patients without a device and found
the prevalence of
C. albicans
to be higher in patients
with xed apparatus, with a statistically signicant
difference in the presence of
C. albicans
in patients
treated with appliances when compared to those
not treated. They also found that the use of a xed
orthodontic appliance alters the state of the oral
cavity, impacting the colonization of the biolm by
opportunistic/pathogenic strains and, consequently,
increasing the risk of its dissemination to various
tissues and organs, emphasizing that the oral cavity
can act as a reservoir of microorganisms that can
induce infections of clinical importance. Having
acknowledged the participation of
C. albicans
biolm in some pathogenic processes, the aim of
this study was to evaluate the biolm formation of
C. albicans
on the surface of orthodontic brackets
of different materials, together with wires and
ligatures.
MATERIAL AND METHODS
Production of biolms
The sample consisted of 300 orthodontic
rods of the upper central incisors of the
straight wire technique, Roth prescription,
with a .022” slot (Morelli®, Sorocaba, Brazil),
and 300 segments of 1 cm wires fastened by
elastomeric and metallic ligatures. Thirty groups
(n=10) were created based on the type of bracket
(conventional metallic/MC, self-ligating brackets/
SLB, ceramic bracket/CB), wire metallic alloy
(Nickel-Chromium/NiCr, Nickel-Titanium/NiTi),
wire size and cross-section (.014”, .018”, .018” x
.025”) and ligatures types (025 mm-stainless steel
ligature/SSL, elastomeric chain/EC) (Table I).
transversal .018”x.025” apresentaram maior formação de biolme quando associados aos três tipos de bráquetes.
Os conjuntos com os de NiCr e ligaduras SSL com bráquetes MC (
p
=0,0008) e CB
(p
=0,0003) apresentaram
maior formação de biolme. Conclusão: bráquetes MC com os de NiTi e NiCr apresentaram menor formação
de biolme, independente da ligadura e secção transversal ou bitola do o e, braquetes MC e CB com os de
NiCr e ligaduras SSL foram mais propensos a acumular biolmes.
PALAVRAS-CHAVE
Biolmes, Candida albicans, Aparelhos ortodônticos xos, Bráquetes ortodônticos, Microscopia eletrônica de
varredura.
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Braz Dent Sci 2023 Apr/Jun;26 (2): e3440
Fernandes EE et al.
Analysis of biofilm formation by Candida albicans in different types of orthodontic fixed appliances and devices
Fernandes EE et al.
Analysis of biofilm formation by Candida albicans in different
types of orthodontic fixed appliances and devices
Biolms were cultured in 24-well culture plates
(TPP®, Trasadingen, Switzerland) containing
different brackets, following the methodology
described by Pereira et al. (2011) [21], with
necessary modications. Suspensions of strains
of
C. albicans
(ATCC 18804) were adjusted to
10
7
cells/mL using a spectrophotometer (B582,
Micronal, São Paulo, Brazil), and 2 mL BHI broth
(Brain Heart Infusion, Difco, Detroit, USA) was
added to each well. The plates were incubated
with shaking at 75 rpm (Quimis, Diadema, Brazil)
for 90 min at 37°C to facilitate initial adhesion.
After the adhesion phase, the suspension was
aspirated and each well was washed with 2 mL
of phosphate-buffered saline (PBS) to remove
non-adherent cells. Subsequently, 2 mL of BHI
broth was added to each well to form a biolm.
All the plates were incubated at 37°C for 48 h with
shaking at 75 rpm. After the incubation period,
the brackets were washed twice with PBS and
the biolms were detached using a Sonopuls HD
2200 ultrasonic homogenizer (Bandelin Electronic,
Berlin, Germany) at 50 W for 30 s. The suspensions
were serially diluted and plated on Sabouraud
dextrose agar (Difco, Detroit, USA) to determine
the colony-forming units per mL (CFU/mL).
Scanning Electron Microscopy (SEM)
After biolms formation, the devices were
fixed in 1 ml of 2.5% glutaraldehyde for 1 h.
Specimens were then dehydrated serially using
increasing concentrations of ethanol (10%, 25%,
50%, 75%, and 90%) for 20 min each, followed by
immersion in 100% ethanol for 1 h. The plates were
kept in an incubator at 37°C for 24 h to permit total
drying of the specimens. After drying, the specimens
were transferred to aluminum stubs and sputter
coated with gold for 160 s at 40 mA (Vacuum Desk
II; Denton Vacuum LLC, Moorestown, NJ, USA).
The specimens were examined and imaged using
a JSM-5600 scanning electron microscope (JEOL
USA, Inc., Peabody, MA).
Statistical analysis
The CFU/mL (log
10
) counts were analyzed
by ANOVA and Tukey’s test using the GraphPad
Prism 6 program (GraphPad Software, Inc., San
Diego, CA, USA), with a signicance level of 5%.
RESULTS
The MC group showed a lower amount of
biolm formation in relation to the SLB and CB
groups, which were very similar to each other
(Figure 1).
Table I - Research groups according to bracket type, arc metal alloy
and ligature type
Group Bracket Archwire Ligature
G1 MC .014” NiTi EC
G2 MC .014” NiTi SSL
G3 MC .018” NiTi EC
G4 MC .018” NiTi SSL
G5 MC .014” NiCr EC
G6 MC .014” NiCr SSL
G7 MC .018” NiCr EC
G8 MC .018” NiCr SSL
G9 MC .018”x.025” NiTi EC
G10 MC .018”x.025” NiTi SSL
G11 MC .018”x.025” NiCr EC
G12 MC .018”x.025” NiCr SSL
G13 CB .014” NiTi EC
G14 CB .014” NiTi SSL
G15 CB .018” NiTi EC
G16 CB .018” NiTi SSL
G17 CB .014” NiCr EC
G18 CB .014” NiCr SSL
G19 CB .018” NiCr EC
G20 CB .018” NiCr SSL
G21 CB .018”x.025” NiTi EC
G22 CB .018”x.025” NiTi SSL
G23 CB .018”x.025” NiCr EC
G24 CB .018”x.025” NiCr SSL
G25 SLB .014” NiTi No ligature
G26 SLB .018” NiTi No ligature
G27 SLB .014” NiCr No ligature
G28 SLB .018” NiCr No ligature
G29 SLB .018”x.025” NiTi No ligature
G30 SLB .018”x.025” NiCr No ligature
Figure 1 - Quantitative analysis of biofilm formation by CFU/mL
count in different types of brackets: Means and standard deviations
of
C. albicans
ATCC18804 CFU/mL (log) values in the following
groups: conventional metallic/MC, self-ligating brackets/SLB,
ceramic bracket/CB. ANOVA and Tukey’s test,
p
≤ 0.05.
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Braz Dent Sci 2023 Apr/Jun;26 (2): e3440
Fernandes EE et al.
Analysis of biofilm formation by Candida albicans in different types of orthodontic fixed appliances and devices
Fernandes EE et al.
Analysis of biofilm formation by Candida albicans in different
types of orthodontic fixed appliances and devices
The amount of biolm formed on different
sets of brackets and wires is shown in Table II.
In general, greater biolm formation by
C. albicans
was observed when .018”x.025” rectangular wires
were used together with brackets. For the MC and
CB brackets, a greater accumulation of biolm
was observed when NiCr wires were used. It was
impossible to identify a greater accumulation of
biolm, for the SLB brackets, when NiCr or NiTi
alloys were used.
In the interaction between the types of
ligatures, brackets, and wires, different amounts
of CFU/mL were observed in the colonization
of
C. albicans
biolms. The combinations that
showed highest biofilm accumulation were
MC-NiCr-SSL and CB-NiCr with both EC and SSL.
The sets that exhibited low biolm formation
were MC-NiCr-EC and CB-NiTi-SSL. There was
a significant difference in biofilm formation
between sets when the types of brackets, MC and
CB were considered (Figure 2).
SEM analysis performed based on these
results, showed that the bracket surfaces had
recesses, sharp angles, grooves, and clips, as in
SLB brackets, that facilitated biolm retention
(Figure 3). In Figure 3C, it is possible to observe
the presence of yeasts and hyphae of
C. albicans
,
mainly in the niches formed by the bracket clip.
Table II – Means and standard deviations of CFU/mL (log
10
) in the tests performed in different types of brackets and archwires
CFU/mL (log
10
)
.014” .018” .018”x .025”
p
value
NiCr
MC 5.076± 0.336 4.871 ± 0.201 5.278 ± 0.091
p
< 0.0001CB 5.309 ± 0.148 5.487 ± 0.108 5.298 ± 0.129
SLB 5.166 ± 0.059 5.416 ± 0.078 5.534 ± 0.145
NiTi
MC 5.300 ± 0.284 4.849 ± 0.308 4.680 ± 0.155
p
< 0.0001CB 4.886 ± 0.212 5.237 ± 0.436 5.240 ± 0.043
SLB 5.310 ± 0.069 5.264 ± 0.126 5.332 ± 0.054
Figure 2 - Quantitative analysis of biofilm formation by CFU/mL count in different types of brackets, wires and ligatures: Means and standard
deviations of
C. albicans
ATCC18804 CFU/mL (log) values in the following groups: conventional metallic/MC and ceramic bracket/CB with
types of wires and ligatures. ANOVA and Tukey’s test,
p
≤ 0.05.
Figure 3 - Scanning electron microscopy images of biofilms formed by
C. albicans
on SLB brackets surfaces, as follows: (A) 80X; (B) 1500X; (C),
3000X magnifications. It is possible to observe the presence of yeasts (
*
), and hyphae ( →) of
C. albicans
.
5
Braz Dent Sci 2023 Apr/Jun;26 (2): e3440
Fernandes EE et al.
Analysis of biofilm formation by Candida albicans in different types of orthodontic fixed appliances and devices
Fernandes EE et al.
Analysis of biofilm formation by Candida albicans in different
types of orthodontic fixed appliances and devices
DISCUSSION
Information about the formation of
C. albicans
biofilms in components of fixed orthodontic
appliances, which hinders oral hygiene and
increases plaque retention, is essential because
this microorganism is present in oral microbiota
and can participate in pathological processes
such as caries [22,23]. This study simulated
xed orthodontic appliances to contribute to the
understanding of the adhesion of
C. albicans
biofilms during orthodontic treatment, which
contributes to the formation of more retentive areas.
The association between
Candida
species
and the establishment of dental caries has been
reported in several works [22-24]. Caries begin
with the formation of biofilms by cariogenic
microorganisms such as
S. mutans
and
C.
albicans
[25]. The interaction between these
microorganisms can be mutualistic, where both
are favored, with a greater ability to adhere to
surfaces when in association [16].
In vitro
studies
suggest that
C. albicans
has a high acidogenic
potential and capacity to cause mineral loss and is
therefore an adjunct in the process of establishing
dental caries [18]. Furthermore, although the
role of
C. albicans
in periodontal disease is not
well established, it is considered an important
pathogen in both the progression and persistence
of this disease [26].
Brackets cause the maintenance of good oral
hygiene difcult and create microbial shelters,
resulting in biofilm build-up. The use of SLB
became widespread, as it did not include elastic
or metallic ligatures and was believed to be more
hygienic [27,28]; however, this hypothesis was
not proven in our study.
Pellegrini et al. (2009) [27] evaluated
biofilm retention during treatment with
conventional brackets in interaction with
rubber band ligations and self-ligated brackets
(In-Ovation R/Mini-Ovation, GAC) and
concluded that patients with self-ligated brackets
had lower biolm rates than those who received
conventional brackets. However, in this study,
the levels of hygiene of the sample were not
considered, and the results from Pellegrini et al.
(2009) [27] study could be inuenced by the
location of collection, which was performed
around the bracket and at the tooth and bracket
interface as opposed to our methodology, which
evaluated the formation of biolms on the entire
surface of the bracket by sonication. However,
corroborating our results, the authors state that
SLB retain more biolm either because they have
more retentive areas [29,30], larger dimensions
and a more complex design [31], or because of
the clip [6,32].
According to Van Gastel et al. (2007) [29],
when analyzing the distribution of the biolm
through the brackets using SEM, irregularities
in the interface between different parts of the
self-ligating brackets were observed. This was
confirmed in our results through the same
analysis. Regardless of the type of bracket, the
authors agree that the slot region closed by the
clip retains the most biolm, probably because it
behaves like a closed tube [6,32].
In this study wires with a round cross-section
(.014” or .018”) did not differ signicantly in
terms of biolm accumulation. The wire with a
rectangular cross-section (.018”x.025”) promoted
greater accumulation of biofilm, probably
because of the formation of more retentive
niches due to the presence of sharper angles
in its conformation. Particularly, in phases of
orthodontic treatment, when it is necessary
to use larger wires, according to our results,
individuals might be more susceptible to biolm
formation and creation of retentive areas, which
suggests that there is a correlation between
biofilm removal and the use of auxiliary and
professional methods to preserve the patient’s
oral health. Thus, the orthodontist needs to pay
greater attention to these parameters.
There was no signicant difference in the
accumulation of biolm between EC and SSL,
corroborating the literature on the presence
of
P. gingivalis
[1]. In some combinations,
one type accumulated more biofilm; in other
combinations, it accumulated less biolm. More
biolm was always observed in combinations
with SLB. When evaluating the retention of
S. mutans
biofilms around MC brackets with
SSL, EC, and SLB brackets, combinations with
EC showed greater biolm accumulation [30].
Through real-time PCR, the authors observed
that the accumulation of
S. mutans
,
S. sobrinus
,
L. casei
, and
L. acidophilus
in MC with SSL and
SLB was similar [33]. Although no ligatures
are used in self-ligated brackets, calcification
of bacterial plaque in the cervical region may
occur [32], making it difcult to open and close
the clip, which can lead to its malfunction. It is
important to adopt effective mechanisms of daily
6
Braz Dent Sci 2023 Apr/Jun;26 (2): e3440
Fernandes EE et al.
Analysis of biofilm formation by Candida albicans in different types of orthodontic fixed appliances and devices
Fernandes EE et al.
Analysis of biofilm formation by Candida albicans in different
types of orthodontic fixed appliances and devices
oral hygiene by the patient and periodically by
the professional to negate these issues [34].
In this study a signicant increase in number
of colonies of
S. mutans
and
C. albicans
in
individuals with fixed orthodontic appliances
and the effectiveness of removing this biolm
through proper brushing was observed. Thus,
even if an individual is undergoing orthodontic
treatment and accessories conducive to greater
accumulation of microorganisms are used, such as
self-ligating brackets and rectangular NiCr wires,
professional prophylaxis and proper instruction
in oral hygiene are essential for a significant
reduction in bacterial plaque, and plaque control
in orthodontic patients is extremely important
for maintaining oral health and preventing
periodontal disease [35,36]. As a relevant adjunct
to more effective oral hygiene, professionals
should guide their patients regarding the daily
use of mouthwashes [37,38].
CONCLUSION
Thus, brackets of MC with NiTi and NiCr
wires showed lower biolm formation, regardless
of the ligature and cross-sectional or gauge of the
wire and, MC and CB brackets with NiCr wires
and SSL ligatures were more likely to accumulate
biolms.
Acknowledgements
The authors are grateful to the Institute of
Science and Technology, São José dos Campos
Campus, São Paulo State University – UNESP and
are grateful to Specialist in orthodontics Thácia
Oliveira Silva for content contributions during
the development of this manuscript.
Author’s Contributions
EEF, DFLMO, RPJ, PAD: Conceptualization.
EEF, DFLMO, RPJ, PAD: Hypothesis. EEF,
DFLMO, RPJ, PAD: Experiments. EEF, DFLMO,
RPJ, PAD, PPB: Writing. PPB: Data tabulation.
PPB: Statistical. AOCJ, WO, SMR: Supervision.
Conict of Interest
No conicts of interest declared concerning
the publication of this article.
Funding
This study was supported by private funding.
Regulatory Statement
The study was waived of ethical approval
because it did not include patients or animals,
only standard microbiological samples acquired
for laboratory studies were used (Candida ATCC).
REFERENCES
1. Türkkahraman H, Sayin MO, Bozkurt FY, Yetkin Z, Kaya S, Onal
S. Archwire ligation techniques, microbial colonization, and
periodontal status in orthodontically treated patients. Angle
Orthod. 2005;75(2):231-6. PMid:15825788.
2. Krishnan V, Davidovitch A. Cellular, molecular, and tissue-level
reactions to orthodontic force. Am J Orthod Dentofacial
Orthop. 2006;129(4):469.E1-32. http://dx.doi.org/10.1016/j.
ajodo.2005.10.007. PMid:16627171.
3. Shukla C, Maurya R, Singh V, Tijare M. Evaluation of role of fixed
orthodontics in changing oral ecological flora of opportunistic
microbes in children and adolescent. J Indian Soc Pedod Prev
Dent. 2017;35(1):34-40. http://dx.doi.org/10.4103/0970-
4388.199226. PMid:28139480.
4. Tufekci E, Dixon JS, Gunsolley JC, Lindauer SJ. Prevalence of
white spot lesions during orthodontic treatment with fixed
appliances. Angle Orthod. 2011;81(2):206-10. http://dx.doi.
org/10.2319/051710-262.1. PMid:21208070.
5. Derks A, Katsaros C, Frencken JE, van’t Hof MA, Kuijpers-
Jagtman AM. Caries-inhibiting effect of preventive measures
during orthodontic treatment with fixed appliances. Caries
Res. 2004;38(5):413-20. http://dx.doi.org/10.1159/000079621.
PMid:15316184.
6. Nascimento LEAG, Pithon MM, Santos RL, Freitas AOA, Alviano
DS, Nojima LI,etal. Colonization of
Streptococcus mutans
on
esthetic brackets: self-ligating vs conventional. Am J Orthod
Dentofacial Orthop. 2013;143(Suppl 4):S72-7. http://dx.doi.
org/10.1016/j.ajodo.2012.07.017. PMid:23540639.
7. Nascimento LEAG, Souza MMG, Azevedo ARP, Maia LC. Are
self-ligating brackets related to less formation of
Streptococcus
mutans
colonies? A systematic review. Dental Press J Orthod.
2014;19(1):60-8. http://dx.doi.org/10.1590/2176-9451.19.1.060-
068.oar. PMid:24713561.
8. Folco AA, Benítez-Rogé SC, Iglesias M, Calabrese D,
Pelizardi C, Rosa A, et al. Gingival response in orthodontic
patients: comparative study between self-ligating and
conventional brackets. Acta Odontol Latinoam. 2014;27(3):120-4.
PMid:25560690.
9. Longoni JN, Lopes BMV, Freires IA, Dutra KL, Franco A, Paranhos
LR. Self-ligating versus conventional metallic brackets on
Streptococcus mutans
retention: a systematic review. Eur J Dent.
2017;11(4):537-47. http://dx.doi.org/10.4103/ejd.ejd_132_17.
PMid:29279684.
10. Contaldo M, Lucchese A, Lajolo C, Rupe C, Stasio D, Romano
A,etal. The oral microbiota changes in orthodontic patients and
effects on oral health: an overview. J Clin Med. 2021;10(4):780.
http://dx.doi.org/10.3390/jcm10040780. PMid:33669186.
11. Hägg U, Kaveewatcharanont P, Samaranayake Y, Samaranayake
L. The effect of fixed orthodontic appliances on the oral carriage
of
Candida
species and
Enterobacteriaceae.
Eur J Orthod.
7
Braz Dent Sci 2023 Apr/Jun;26 (2): e3440
Fernandes EE et al.
Analysis of biofilm formation by Candida albicans in different types of orthodontic fixed appliances and devices
Fernandes EE et al.
Analysis of biofilm formation by Candida albicans in different
types of orthodontic fixed appliances and devices
2004;26(6):623-9. http://dx.doi.org/10.1093/ejo/26.6.623.
PMid:15650072.
12. Beerens M, Cate JMT, van der Veen MH. Microbial profile
of dental plaque associated to white spot lesions in
orthodontic patients immediately after the bracket removal.
Arch Oral Biol. 2017;78:88-93. http://dx.doi.org/10.1016/j.
archoralbio.2017.02.011. PMid:28222388.
13. Dalazen D, Zanrosso D, Wanderley L, Silva NL, Fuentefria AM.
Comparação do perfil de suscetibilidade entre isolados clínicos
de
Candida spp
. orais e vulvovaginais no Sul do Brasil. J Bras
Patol Med Lab. 2011;47(1):33-8. http://dx.doi.org/10.1590/
S1676-24442011000100004.
14. Szabó B, Majoros L, Papp-Falusi E, Szabó Z, Szabó J, Márton
I,et al. Studies on the possible aetiological role of different
Candida
species in pathogenesis of dentine caries by monitoring
the calcium release from tooth particles. Acta Microbiol
Immunol Hung. 2014;61(1):11-7. http://dx.doi.org/10.1556/
amicr.61.2014.1.2. PMid:24631750.
15. Branting C, Sund ML, Linder LE. The influence of
Streptococcus
mutans
on adhesion of
Candida albicans
to acrylic surfaces
in vitro. Arch Oral Biol. 1989;34(5):347-53. http://dx.doi.
org/10.1016/0003-9969(89)90108-8. PMid:2532001.
16. Barbieri DSV, Vicente VA, Fraiz FC, Lavoranti OJ, Svidzinski TIE,
Pinheiro RL. Analysis of the in vitro adherence of
Streptococcus
mutans
and
Candida albicans.
Braz J Microbiol. 2007;38(4):624-
31. http://dx.doi.org/10.1590/S1517-83822007000400009.
17. Nikawa H, Yamashiro H, Makihira S, Nishimura M, Egusa H,
Furukawa M, et al. In vitro cariogenic potencial of
Candida
albicans.
Mycoses. 2003;46(11-12):471-8. http://dx.doi.
org/10.1046/j.0933-7407.2003.00888.x. PMid:14641620.
18. Charone S, Portela MB, Chagas MS, Soares RMA, Castro GFB.
Biofilm of
Candida albicans
from oral cavity of an HIV-infected
child: challenge on enamel microhardness. Oral Surg Oral
Med Oral Pathol Oral Radiol. 2013;115(4):500-4. http://dx.doi.
org/10.1016/j.oooo.2012.11.003. PMid:23380483.
19. Klinke T, Guggenheim B, Klimm W, Thurnheer T. Dental
caries in rats associated with
Candida albicans.
Caries Res.
2011;45(2):100-6. http://dx.doi.org/10.1159/000324809.
PMid:21412001.
20. Perkowski K, Baltaza W, Conn DB, Marczyńska-Stolarek M,
Chomicz L. Examination of oral biofilm microbiota in patients
using fixed orthodontic appliances in order to prevent risk
factors for health complications. Ann Agric Environ Med.
2019;26(2):231-5. http://dx.doi.org/10.26444/aaem/105797.
PMid:31232051.
21. Pereira CA, Romeiro RL, Costa ACBP, Machado AKS, Junqueira JC,
Jorge AOC. Susceptibility of
Candida albicans, Staphylococcus
aureus
, and
Streptococcus mutans
biofilms to photodynamic
inactivation: an in vitro study. Lasers Med Sci. 2011;26(3):341-8.
http://dx.doi.org/10.1007/s10103-010-0852-3. PMid:21069408.
22. Metwalli KH, Khan SA, Krom BP, Jabra-Rizk MA.
Streptococcus
mutans, Candida albicans
, and the human mouth: a sticky
situation. PLoS Pathog. 2013;9(10):e1003616. http://dx.doi.
org/10.1371/journal.ppat.1003616. PMid:24146611.
23. Sztajer H, Szafranski SP, Tomasch J, Reck M, Nimtz M, Rohde
M, et al. Cross-feeding and interkingdom communication in
dual-species biofilms of
Streptococcus mutans
and
Candida
albicans.
ISME J. 2014;8(11):2256-71. http://dx.doi.org/10.1038/
ismej.2014.73. PMid:24824668.
24. Cerqueira DF, Portela MB, Pomarico L, Soares RMA, Souza
IPR, Castro GF. Oral
Candida
colonization and its relation
with predisposing factors in HIV-infected children and their
uninfected siblings in Brazil: the era of highly active antiretroviral
therapy. J Oral Pathol Med. 2010;39(2):188-94. http://dx.doi.
org/10.1111/j.1600-0714.2009.00857.x. PMid:20040023.
25. Ikono R, Vibriani A, Wibowo I, Saputro KE, Muliawan W,
Bachtiar BM,etal. Nanochitosan antimicrobial activity against
Streptococcus mutans
and
Candida albicans
dual-species
biofilms. BMC Res Notes. 2019;12(1):383. http://dx.doi.
org/10.1186/s13104-019-4422-x. PMid:31287001.
26. Jabri B, Iken M, Achmit M, Rida S, Ennibi O. Occurrence of
Candida albicans
in Periodontitis. Int J Dent. 2021;2021:5589664.
http://dx.doi.org/10.1155/2021/5589664. PMid:34135968.
27. Pellegrini P, Sauerwein R, Finlayson T, McLeod J, Covell D Jr, Maier
T,etal. Plaque retention by self-ligating vs elastomeric orthodontic
brackets: quantitative comparison of oral bacteria and detection
with adenosine triphosphate-driven bioluminescence. Am J
Orthod Dentofacial Orthop. 2009;135(4):426-E1-7. http://dx.doi.
org/10.1016/j.ajodo.2008.12.002. PMid:19361723.
28. Jing D, Hao J, Shen Y, Tang G, Lei L, Zhao Z. Effect of fixed
orthodontic treatment on oral microbiota and salivary proteins.
Exp Ther Med. 2019;17(5):4237-43. http://dx.doi.org/10.3892/
etm.2019.7401. PMid:30988796.
29. Van Gastel J, Quirynen M, Teughels W, Coucke W, Carels
C. Influence of bracket design on microbial and periodontal
parameters in vivo. J Clin Periodontol. 2007;34(5):423-31. http://
dx.doi.org/10.1111/j.1600-051X.2007.01070.x. PMid:17448045.
30. Garcez AS, Suzuki SS, Ribeiro MS, Mada EY, Freitas AZ, Suzuki
H. Biofilm retention by 3 methods of ligation on orthodontic
brackets: a microbiologic and optical coherence tomography
analysis. Am J Orthod Dentofacial Orthop. 2011;140(4):e193-8.
http://dx.doi.org/10.1016/j.ajodo.2011.04.019. PMid:21967957.
31. Jung WS, Kim K, Cho S, Ahn SJ. Adhesion of periodontal pathogens
to self-ligating orthodontic brackets: an in-vivo prospective
study. Am J Orthod Dentofacial Orthop. 2016;150(3):467-75.
http://dx.doi.org/10.1016/j.ajodo.2016.02.023. PMid:27585775.
32. Pithon MM, Santos RL, Nascimento LE, Ayres AO, Alviano D,
Bolognese AM. Do self-ligating brackets favor greater bacterial
aggregation? Braz J Oral Sci. 2011;10(3):208-12.
33. Baka ZM, Basciftci FA, Arslan U. Effects of 2 bracket
and ligation types on plaque retention: a quantitative
microbiologic analysis with real-time polymerase chain reaction.
Am J Orthod Dentofacial Orthop. 2013;144(2):260-7. http://
dx.doi.org/10.1016/j.ajodo.2013.03.022. PMid:23910207.
34. Sallum EJ, Nouer DF, Klein MI, Gonçalves RB, Machion L,
Sallum AW,et al. Clinical and microbiologic changes after
removal of orthodontic appliances. Am J Orthod Dentofacial
Orthop. 2004;126(3):363-6. http://dx.doi.org/10.1016/j.
ajodo.2004.04.017. PMid:15356501.
35. Souza RA, Magnani MBBA, Nouer DF, Silva CO, Klein MI, Sallum
EA,etal. Periodontal and microbiologic evaluation of 2 methods
of archwire ligation: ligature wires and elastomeric rings. Am J
Orthod Dentofacial Orthop. 2008;134(4):506-12. http://dx.doi.
org/10.1016/j.ajodo.2006.09.067. PMid:18929268.
36. Penoni DC, Moura MF, Florenzano LGC, Santos MM, Carlos
JC. The impact of oral hygiene instruction on plaque control
in orthodontic patients: a cross-sectional study. Braz Dent
Sci. 2022;25(4):e3557. http://dx.doi.org/10.4322/bds.2022.
e3557.
37. Pithon MM, Sant’Anna LI, Baião FC, Santos RL, Coqueiro RS,
Maia LC. Assessment of the effectiveness of mouthwashes in
reducing cariogenic biofilm in orthodontic patients: a systematic
review. J Dent. 2015;43(3):297-308. http://dx.doi.org/10.1016/j.
jdent.2014.12.010. PMid:25572792.
38. Paulone S, Malavasi G, Ardizzoni A, Orsi CF, Peppoloni S, Neglia
RG,etal.
Candida albicans
survival, growth and biofilm formation
are differently affected by mouthwashes: an in vitro study. New
Microbiol. 2017;40(1):45-52. PMid:28217816.
8
Braz Dent Sci 2023 Apr/Jun;26 (2): e3440
Fernandes EE et al.
Analysis of biofilm formation by Candida albicans in different types of orthodontic fixed appliances and devices
Fernandes EE et al.
Analysis of biofilm formation by Candida albicans in different
types of orthodontic fixed appliances and devices
Sigmar de Mello Rode
(Corresponding address)
Universidade Estadual Paulista “Júlio de Mesquita Filho”, Instituto de Ciência e
Tecnologia, Departamento de Materiais Odontológicos e Prótese, São José dos
Campos, SP, Brazil.
Email: sigmar.rode@unesp.br
Date submitted: 2022 Mar 16
Accept submission: 2022 Nov 21