Hindawi

International Journal of Dentistry

Volume 2021, Article ID 5589664, 7 pages
https://doi.org/10.1155/2021/5589664

Research Article
Occurrence of Candida albicans in Periodontitis

Brahim Jabri ,1 Maryem Iken ,2 Mohamed Achmit ,3 Sana Rida ,4

and Oum Keltoum Ennibi 5
1
Research Laboratory in Oral Biology and Biotechnology, Faculty of Dental Medicine of Rabat,
Mohammed V University in Rabat, Rabat, Morocco
2
Clinical Biology Department, Faculty of Medicine and Pharmacy, Mohammed V University in Rabat, Rabat, Morocco
3
Laboratory of Virology, Microbiology and Quality/ Eco-toxicology and Biodiversity,
Faculty of Sciences and Techniques Mohammedia, University Hassan II Casablanca, Casablanca, Morocco
4
Department of Conservative Dentistry, Faculty of Dental Medicine of Rabat, Mohammed V University in Rabat, Rabat, Morocco
5
Department of Periodontology, Faculty of Dental Medicine of Rabat, Mohammed V University in Rabat, Rabat, Morocco

Correspondence should be addressed to Oum Keltoum Ennibi; o.ennibi@um5s.net.ma

Received 6 January 2021; Revised 22 April 2021; Accepted 22 May 2021; Published 29 May 2021

Academic Editor: Lucio Goncalves

Copyright © 2021 Brahim Jabri et al. This is an open access article distributed under the Creative Commons Attribution License,
which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Background. Periodontal diseases are the result of an imbalance between the microbiota and immune defense. The role of yeast in
the pathogenesis of these diseases has been studied. This study aims to assess the occurrence of Candida albicans in periodontitis.
Materials and Methods. Fifty subjects were recruited for the study (15 healthy individuals and 35 periodontitis subjects). The
periodontal examination and plaque sampling were carried out for all patients. Candida albicans identification was based on
culture, direct examination, and polymerase chain reaction. The statistical analysis was performed by SPSS 20 (SPSS Inc., Chicago,
IL, USA). Results. Twenty percent of the diseased group harbored Candida albicans which was slightly higher than in the healthy
group (7%), suggesting that, under normal conditions, yeast does not grow easily in subgingival sites. However, no significant
difference between the healthy and periodontitis groups (p � 0.23) was found. Our results also indicated that the presence of
Candida albicans was neither gender nor age related in the studied groups. Conclusion. The results of this study suggest that
Candida albicans occurs in periodontitis. More studies are needed to clarify the potential role of this yeast in different stages and
forms of the disease.

1. Introduction of the microflora associated with periodontal disease. In-

deed, various microorganism species, including Gram-
Among Candida species, Candida albicans is the most negative anaerobic bacteria organized in a complex biofilm,
widespread yeast associated with healthy and pathologic oral have been associated with the initiation and progression of
conditions [1, 2]. Indeed, this opportunist microorganism periodontitis [7]. Porphyromonas gingivalis, Tannerella
belongs to commensal microflora in the healthy human forsythia, and Treponema denticola, known as the “red
digestive tract, but can become pathogenic under the in- complex” together with Aggregatibacter actino-
fluence of general or local favorable factors. mycetemcomitans have been identified as the most peri-
Periodontitis is a worldwide oral disease with a very opathogenic bacteria associated with different forms of
complex etiopathogenesis, including dysbiosis and host periodontitis worldwide [7, 8]. Lately, some studies dis-
immune responses that comaintain conditions for the oc- cussed also the possible role of viruses [9, 10] and yeasts in
currence of periodontal disease in susceptible individuals periodontitis pathogenesis [11, 12]. Thus, as the disease
[3, 4]. Clinically, periodontitis involves attachment loss breaks through, the periodontal pockets become the re-
around teeth, forming periodontal pockets, and bone de- ceptacle of a large number of microorganisms including
struction [5, 6]. Several studies have raised the heterogeneity C. albicans [6, 13, 14]. Nevertheless, the role of this yeast in
2 International Journal of Dentistry

the pathogenesis of periodontal disease remains unclear. The evidence of progression rate in three categories: slow (grade
aim of the present study is to assess the presence of Candida A), moderate (grade B), and rapid progression (grade C).
albicans in periodontitis.

2. Materials and Methods 2.2.2. Plaque Sampling. A pool of subgingival biofilm

samples were collected from four sites (one site per quad-
2.1. Study Population. Fifty subjects were recruited from the rant) in each patient. We selected the deepest site in each
clinical department of Periodontology, “Center of Consul- quadrant with a pocket depth equal or greater than 5 mm
tation and Dental Treatment,” Ibn Sina University Hospital (PPD≥ 5 mm), clinical attachment loss ≥2 mm, and which
of Rabat, Morocco (CCTD-CHIS, Rabat). were bleeding on probing.
The approval for the study was obtained from the Re- Plaque sampling was obtained by introducing a sterilized
search Ethics Committee of Mohammed V University, absorbent paper point (30 mm diameter) into the gingival
Rabat, Morocco (Ethical agreement number 102/19). All sulcus for 20 seconds (SURE DENT CORPORATION; CEO
subjects were informed and signed the informed consent. 197). The samples were placed in 2 mL of sterile phosphate
The inclusion criteria included patients in good general buffered saline (PBS) as a transport medium and immedi-
health, aged 18 years and above, with at least 20 teeth ately transferred to the laboratory for analysis.
present, and who have not received any periodontal treat-
ment or antibiotic medication during at least the previous six
2.2.3. Yeast Culture. Samples were first processed and
months prior to the study. The exclusion criteria included
cultured. They were dispersed and plated onto a sabouraud
patients under orthodontic treatment, those who smoke or
chloramphenicol medium for the isolation of yeasts. Plates
chew any other kind of tobacco, diabetic patients, those
were incubated at 37°C in non-CO2 atmosphere for 24 to 48
having symptomatic oral candidosis and/or had been under
hours [17, 18]. The plates were checked daily for yeast
antifungal treatment, and pregnant and lactating women.
growth.
Identification was based on colony and cellular mor-
2.2. Methods phology. Candida albicans colonies on the Sabouraud
chloramphenicol medium are creamy whitish and smooth
2.2.1. Periodontal Examination. Prior to the periodontal [19] (Figure 1).
examination, all patients signed the informed consent forms. Under direct examination: Candida yeasts appear as
The assessed clinical variables were modified gingival index oval, ovoid, or elongated and possibly budding elements [20]
(GI), plaque index (PI) [15], probing pocket depth (PPD), (Figure 2).
and clinical attachment loss (CAL). Probing pocket depth Pure cultures of yeast colonies were identified and
and attachment loss were measured using a standard confirmed later as Candida albicans by PCR.
periodontal probe (Hu-friedy, Chicago, IL), at six sites per
tooth, i.e., distobuccal, buccal, mesiobuccal, distolingual,
lingual, and mesiolingual, in all teeth excluding third molars. 2.2.4. Identification of Candida albicans by PCR.
A set of full-mouth standardized intraoral radiographs was Genomic DNA was extracted as follows: 4 to 6 yeast colonies
obtained from each patient. were suspended in 1 ml of sterile 0.9% NaCl. The extraction
Based upon clinical parameters, radiograph information, was performed using a commercially available BIOLINE
and patient age, we came to the clinical diagnosis based on DNA extraction kit (ISOLATE II GENOMIC DNA KIT,
the classification of the American Academy of Periodon- USA) according to the manufacturer’s instructions. The
tology (AAP) [16]. microtubes were centrifuged at 5000 g for 10 min. Then, the
Thus, in the healthy periodontium, there was no at- supernatant was removed and washed once with 2 mM
tachment loss, no periodontal pocket, no bone loss, and EDTA (pH 8) and centrifuged for 10 min at 5000 g. The
periodontal probing was ≤ 3 mm, whereas periodontitis was supernatant was discarded while the resulting pellet was
defined as having interdental clinical attachment lost de- stored. The extracted DNA was stored at −20°C for later use.
tectable on at least 2 nonadjacent teeth or the presence of Molecular identification of the identified and purified yeast
buccal or oral CAL ≥3 mm with pocketing ≥3 mm detectable strains was accomplished by using the following specific primers
at least in 2 teeth, but not associated with non-periodontitis- for C. albicans detection, generating an amplicon of 500
related causes (i.e., deep dental caries, CAL on a distal site of base pairs (forward: 5′-TGCTTCAGTGTCAGTTATACCT-3′,
a second molar and associated with malposition or resulting Reverse: 5′-ACTGCTCAAACCATCTCTGG-3′) [20].
from a third molar extraction, endodontic lesion draining PCR amplification was performed in a 25 μL reaction
through the marginal periodontium, and a vertical root mixture containing the abovementioned primers (10 μM
fracture). Furthermore, periodontitis patients were classified each), 100 ng of extracted DNA, 100 μM of each of the four
by stage and grade based on the classification. Stages were deoxyribonucleoside triphosphates (dATP, dCTP, dGTP,
defined based on severity (primarily periodontal breakdown and dTTP), 0.5 U of taq DNA polymerase, and 5 mM of
and periodontitis-associated tooth loss) and complexity of buffer.
management (pocket depth, infrabony defects, tooth mo- The PCR amplification parameters were as follows: an
bility, furcation status, and masticatory disturbance). Grades initial denaturation of 1 min at 95°C, followed by 35 cycles of
of periodontitis were estimated based on direct or indirect denaturation of 15 seconds at 95°C, a hybridization of 20
International Journal of Dentistry 3

average age was 31 ± 11 years. Fifteen individuals aged be-

tween 21 and 52 years were healthy, and 35 patients aged
between 18 and 62 years were identified as having peri-
odontitis; however, there was no statistically significant
difference between the two groups. Demographic and
clinical characteristics of the study population are sum-
marized in Table 1.
In the periodontitis group, subgroups were identified
regarding staging and grade. Thus, the patients were diagnosed
as having periodontitis stage II or III and grade B or C. The
statistical analysis showed no significant difference between
periodontitis stage II and III regarding the average age.
However, age was lower in patients who had grade C
periodontitis in comparison with those who had grade B, and
the difference was statistically significant (Tables 2 and 3).
Figure 1: Macroscopic appearance of the Candida species on the The growth of yeast colonies was recorded as a positive
sabouraud chloramphenicol culture medium. growth and the subject as a positive carrier. Among the 17
positive cultures, height isolates were identified as
C. albicans by PCR (one healthy subject and 7 periodontitis
patients) (Figure 3).
The presence of C. albicans was studied among the
periodontitis population according to periodontal status. No
significant differences were found between different groups
(Table 4).
Analysis of the presence of Candida albicans between
subgroups in the periodontitis group did not show any
statistical difference neither when comparing stages II and
III (33.3% and 17.2%, respectively, p � 0.370) nor when
comparing grades Band C (21.0% and 18.7%, respectively,
p � 0.865).

4. Discussion
Figure 2: Appearance of yeast in a fresh culture (×40). Microbial-flora-associated periodontitis is very complex and
has been continuously studied for many years. However, it
should be emphasized that even if bacteria are considered as
seconds at 50°C, and an elongation of 15 seconds at 72°C,
a primary agent in periodontal pathogenesis, other micro-
with a final elongation of 3 min at 72°C. The PCR products
organisms, e.g., viruses and yeasts, are increasingly involved
were analyzed by 1% agarose gel electrophoresis in the
presence of a Dna Ladder 200 bp (Bioline) and visualized by in the microbial etiology of periodontal diseases.
Candida albicans, the most widespread yeast in the oral
using a UV transilluminator system G-Box (Syngene ). ™ cavity, can be isolated in healthy subjects without any clinical
manifestation. It colonizes commonly the tongue [1]. However,
2.2.5. Statistical Analysis. The statistical analysis was per- many studies reported its presence in the healthy periodontium
formed with a statistical program SPSS 20 (SPSS Inc., too. In the present study, 7% of the periodontal healthy patients
Chicago, IL, USA). For each group, continuous variables harbored C. albicans in the subgingival plaque. These results are
with normal distribution were presented as mean ± standard high in comparison to those reported by Urzúa et al. [21], which
deviation (age, depths of periodontal pockets, and attach- reported a prevalence of 3.57% in a population of 28 healthy
ment loss), and categorical variables were given as per- subjects [21]. Meanwhile, Canabaro et al. [22] reported that
centage. Chi-square Pearson’s test was performed to 14.28% of 20 examined healthy subjects were yeast positive.
compare the variables between two independent groups, and Other studies showed variable occurrence (16% to 36%) of
Student’s t test was performed to compare the means of the C. albicans in the subgingival plaque of the healthy perio-
independent samples. The statistical significance threshold dontium [11, 23–25]. In immunocompetent subjects,
used was p < 0.05. C. albicans exists as a minor component of the oral biofilm [26].
It has been suggested also that its presence in the subgingival
3. Results area could be transient [27]. However, it can also exist in
periodontal pockets, and its role in periodontal pathogenesis is
Fifty subjects accepted to participate to the study and fully fit not yet clear.
the inclusion criteria. Thirty-seven (74%) among this pop- In the present study, 20% of periodontitis patients were
ulation were female, and thirteen (26%) were male. The positive for C. albicans. Almost the same result had been
4 International Journal of Dentistry

Table 1: Demographic and clinical characteristics of the study population.

Healthy (n � 15; 30%) Periodontitis (n � 35; 70%) Total (n � 50; 100%) p value
Gender (male/female) 5/10 8/27 13/37 p � 0.439
Age (years) (mean ± SD) 28.73 ± 9.24 33.31 ± 12.16 31.94 ± 11.47 p � 0.199
Plaque index (mean ± SD) 0.21 ± 0.10 2.41 ± 0.69 1.75 ± 1.17 p ≤ 0.001
Gingival index (mean ± SD) 0.05 ± 0.04 2.48 ± 0.68 1.75 ± 1.26 p ≤ 0.001
Pocket depth (mean ± SD) 2.80 ± 0.35 5.79 ± 1.83 4.90 ± 2.07 p ≤ 0.001
Clinical attachment loss (mean ± SD) — 4.61 ± 1.24 — —

Table 2: Comparison of clinical parameters in the periodontitis group according to stages II and stage III.
Periodontitis group (n � 35)
Stage II (n � 6; 17%) Stage III (n � 29; 83%) p value
Age (mean ± SD) 33.00 ± 7.23 33.38 ± 13.04 0.946
Periodontal pockets depths (PPD) (mean ± SD) 5.00 ± 0.44 5.96 ± 1.97 0.251
Clinical attachment loss (CAL) (mean ± SD) 3.17 ± 0.2 4.91 ± 1.15 0.001

Table 3: Comparison of clinical parameters in the periodontitis group according to grade B and grade C.
Periodontitis group (n � 35)
Grade B (n � 19; 54%) Grade C (n � 16; 46%) p value
Age (years) (mean ± SD) 41.89 ± 8.73 23.13 ± 6.31 0.000
Periodontal pockets depths (PPD) (mm) (mean ± SD) 4.78 ± 1.39 7.00 ± 1.56 0.000
Clinical attachment loss (CAL) (mm) (mean ± SD) 4.12 ± 0.73 5.20 ± 1.47 0.008

Figure 3: Agarose gel electrophoresis of PCR products of Candida albicans isolates.

Table 4: The presence of Candida albicans among the study population according to periodontal status.
Candida albicans
p value
Negative carriers (n � 28; 80%) Positive carriers (n � 7; 20%)
Female 21 (78%) 06 (22%)
Gender 0.484
Male 07 (87.5%) 01 (12.5%)
Age (years) (mean ± SD) 32.02 12.19 31.50 7.07 0.907
Plaque index (mm)
2.37 ± 0.75 2.59 ± 0.34 0.460
(mean ± SD)
Gingival index (mm)
2.47 ± 0.74 2.51 ± 0.39 0.907
(mean ± SD)
Periodontal pocket depth
6.07 ± 1.87 4.68 ± 1.20 0.072
(PPD) (mm) (mean ± SD)
Clinical attachment loss
4.81 ± 1.29 3.82 ± 0.55 0.059
(mm) (mean ± SD)
International Journal of Dentistry 5

found by Dahlén [28], who reported a prevalence of 17% and induce inflammation [36]. C. albicans may have some vir-
suggested that this yeast was more common in periodontitis ulence factors such as aspartyl proteinase (SAPs), phos-
patients than in healthy people. Nevertheless, no significant pholipases, and exoenzymes which disturb the locally
differences were found between these two groups (p > 0.05) immune response by the inhibition of polymorphonuclear
in the present study. neutrophil phagotocytosis and induce indirectly inflam-
Relatively few studies have analyzed the possible role of matory reactions [24, 36, 37].
Candida albicans in periodontitis [23, 24, 27]. Matić Petrović When comparing the presence of C. albicans regarding
et al. [25] reported that there is no impact of periodontal gender, 19% and 8%, respectively, of women and men were
pocket depth on the presence of subgingival yeast. However, yeast positive. These results are the same as those reported by
it should be pointed out that the mean probing depth in their Reynaud et al. [24] who showed a prevalence of 20.3%
study was 2.89 ± 0.944 for periodontitis patients compared among women compared to 8.2% in men. Nevertheless, as
to 2.02 ± 0.524 as the mean probing depth in healthy shown previously by Canabaro et al. [22], the presence of
periodontium subjects. Candida albicans is not gender related (p � 0.342).
Many studies showed an association between sub-
gingival colonization by yeast subspecies, including Can- 5. Conclusions
dida albicans, and the presence of severe periodontitis
[6, 28]. Jarvensivu et al. [29] showed a prevalence of 16% in Candida albicans was present in periodontitis patients in this
a population of 25 patients with chronic periodontitis. study. However, no statistical differences were found be-
C. albicans remains the most common fungal pathogen tween the studied groups. Even if the role of C. albicans in
found in patients with periodontitis [21, 22]. In the present periodontal disease has not yet been established, this yeast is
study and according to the new classification of periodontal considered an important pathogen in the progression and
diseases and conditions, the periodontitis group included 2 persistence of this disease. Thus, it would be interesting to
distinguished subgroups based onstage case definition: study in depth the virulence factors and carry out in vitro
stage II and stage III. No statistical difference was seen studies to better understand the potential role of this yeast in
between stage II and stage III, regarding neither age nor the this pathology and, especially, in refractory periodontal
presence of Candida albicans. When comparing the peri- diseases.
odontitis group based on grade, two subgroups were dis-
tinguished, a grade B group and grade C group. A Data Availability
significant difference was found for the average age be-
tween the two groups. Indeed, patients with grade C All data used to support the findings of the study are in-
periodontitis were younger, and the estimate rate of cluded in the article.
periodontitis progression was rapid in comparison with
group B periodontitis patients. However, there was no Conflicts of Interest
significant difference between these grade subgroups when
considering the presence of Candida albicans. Thus, the The authors declare that they have no conflicts of interest.
present study suggests that the presence of Candida albi-
cans in the periodontitis group seems not to be related to
Acknowledgments
the stage or the grade. Nonetheless, these results must be
considered with caution because of the small size of the This work was supported by “Centre National pour la
study population. Moreover, all included patients were Recherche Scientifique et Technique, Morocco (CNRST),”
subjects seeking treatment in a hospital structure. Thus, under Grant no. PPR16/2016. The funder had no role in the
further well-designed study, including a bigger size pop- study’s design, data collection and analysis, the decision to
ulation, is needed to assess and understand the real con- publish, or the preparation of the manuscript.
tribution of Candida albicans in the modified microbiome
associated with periodontitis.
The role of C. albicans in periodontitis pathogenesis is
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