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ORIGINAL ARTICLE
The role of Candida albicans hyphae and Lactobacillus
in denture-related stomatitis
Hakan Bilhan &Tonguç Sulun &Gonca Erkose &
Hanefi Kurt &Zayre Erturan &Omer Kutay &
Tayfun Bilgin
Received: 26 May 2008 / Accepted: 4 December 2008 /Published online: 20 December 2008
#Springer-Verlag 2008
Abstract Denture-related stomatitis (DRS) is still a dilem-
ma in removable prosthodontics. The aim of this study was
to investigate the relationship of DRS with the presence
of Candida albicans hyphae and Lactobacillus. A total of
91 patients wearing maxillary and mandibular complete
dentures were included in the present study and tested
mycologically as well as bacteriologically. A statistically
significant association of DRS was found with denture age
(p=0.003) and continuous denture wearing (p=0.015).
Presence of C. albicans hyphae was shown to be signifi-
cantly higher in DRS cases (p<0.01), and there was a
statistically significant positive correlation between presence
of hyphae and C. albicans (p<0.01). Another interesting
finding was that DRS patients showed higher Lactobacillus
counts in their saliva (p=0.04), as well as in the palate (p=
0.028). C. albicans is an important factor in the development
of DRS. Hyphae seem to facilitate the rise of C. albicans
counts and be related to the inflammatory response of the
tissues. Lactobacillus seems to play an important role in the
presence of DRS, as well. In agreement with many other
studies, the results of this study confirm the importance of
denture age and continuous denture wearing in the develop-
ment of DRS.
Keywords Denture stomatitis .Hyphae .Candida .
Lactobacillus .Denture age .Continuous denture wearing
Introduction
Denture-related stomatitis (DRS) is a common inflamma-
tory process that mainly involves the palatal mucosa when
it is covered by complete dentures [10,33,36,46]. The
etiology appears to be multifactorial; old age and the
associated decline of the immune defense, systemic diseases,
continuous denture wearing, increased age of denture, and
lack of denture cleanliness resulting in the accumulation of
plaque on the denture have all been proposed as predisposing
factors [10,12,21,33,36,43,45,46].
Besides the above-mentioned predisposing factors,
several studies have demonstrated an association between
Candida albicans and DRS [5,6,8,9,18,25,35,38,41].
In comparison with other species of Candida such as Candida
tropicalis,Candida glabrata,Candida parapsilosis,and
Candida krusei,C. albicans was shown to have a very high
occurrence in the oral cavity [1,3,27,49,50]; thus, the
majority of candidiasis still seems to be caused by C.
albicans [16,31,32,48]. According to the results of many
Clin Oral Invest (2009) 13:363–368
DOI 10.1007/s00784-008-0240-6
H. Bilhan (*):T. Sulun :H. Kurt :O. Kutay :T. Bilgin
Faculty of Dentistry, Department of Removable Prosthodontics,
Istanbul University,
34390 Çapa,
Istanbul, Turkey
e-mail: bilhan@istanbul.edu.tr
T. Sulun
e-mail: tsulun@istanbul.edu.tr
H. Kurt
e-mail: hkurt@istanbul.edu.tr
O. Kutay
e-mail: kutayomer@yahoo.com
T. Bilgin
e-mail: tbilgin@turk.net
G. Erkose :Z. Erturan
Faculty of Medicine, Department of Microbiology,
Istanbul University,
Istanbul, Turkey
G. Erkose
e-mail: goncaerkose@yahoo.com
Z. Erturan
e-mail: zerturantr@yahoo.com
studies showing a high incidence of C. albicans in the saliva
of DRS patients in comparison to the control groups, it has
been speculated that its presence is an important factor in the
development of the disease. The higher prevalence of C.
albicans was explained by the higher capability to adhere to
mucosal surfaces, which is considered as the first step in the
pathogenesis of oral candidiasis [19]. C. albicans forms
complex biofilms consisting of a basal blastospore layer
covered by a thick matrix composed of extracellular material
and hyphal elements, which is thicker than less commonly
pathogenic species, including C. parapsilosis,C. glabrata,
and C. tropicalis [26]. Candida, which is primarily found in
the plaque on the tissue surface of the denture rather than on
or in the inflamed mucosa, produce toxins which act as
chemical irritants [18]. However, an important amount of
subjects with C. albicans in their saliva had no symptoms of
DRS. Consequently, there must be factors that are important
in the development of the disease besides the presence of C.
albicans. A striking feature of C. albicans biology is its
ability to grow in a variety of morphological forms. These
range from unicellular yeast to true hyphae. Cellular differ-
ences between pseudohyphae and hyphae are revealed by
septin localization [30]. This property of C. albicans could
promote tissue penetration during the early stages of
infection [48]. Hyphae have been observed to adhere to
and invade host tissues more readily than the yeast form,
suggesting that filamentous growth may contribute to the
virulence of this major human pathogen [29]. The property
of Candida species to adhere to mucosal surfaces is reported
to be enhanced especially by the transition from blastospores
to hyphae [2] and consequently contributing to the virulence
of this pathogen [29].
There are also studies revealing the importance of mutans
streptococci and lactobacilli in the development of DRS [2,7].
It is shown that subjects with a healthy lifestyle generally
have better oral hygiene and thus lower Lactobacillus counts
and less occurring denture stomatitis [45].
The purpose of this study has been to assess the
importance of lactobacilli and the hyphae form of C.
albicans in the etiology of DRS.
Materials and methods
In the period between 2004 and 2007, edentulous patients
attending the Department of Removable Prosthodontics of
Istanbul University, for a new denture, were examined and
interviewed. Out of 108 patients who were wearing complete
dentures longer than 6 months and showing various levels of
DRS symptoms, a total of 71 voluntary patients were
selected to include in our study group. Additionally, 20
subjects without any inflammatory occurrence on the palate
were chosen as the control group. The criterion in the
selection of the control group was, as in the study group, that
the patient wore upper and lower complete dentures for a
period longer than 6 months. The protocol of the whole
project was reviewed by the Ethical Committee of Istanbul
University, and each subject signed an informed consent
form. The patients’age, gender, existence of a denture
actually being used, denture age, frequency, and method of
denture cleaning and dental history were recorded. Clinical
examination was performed by the same investigator for
standardization reasons. The type of dentures, presence, and
localization of denture induced stomatitis.
In the case of DRS, the erythema was scored by using
Newton’s classification index [37]:
1. Slight inflammation (localized slight hyperemia)
2. Moderate inflammation (generalized erythema)
3. Severe inflammation (diffuse and papillary hyperplasia)
For the recording of the denture cleanliness, a subjective
denture hygiene index was used to score the plaque at the
intaglio surface in three groups.
1. Good: no or very little plaque
2. Fair: less than half of the denture base covered by
plaque
3. Poor: more than half of the denture base covered by
plaque
Collecting samples
In order to provide standardization for collected samples,
the overall investigation was carried out at midmorning and
at least 2 h after eating, drinking, or any hygiene procedure.
From each patient, DRS cases as well as the control group,
oral swab samples were collected from a triangular area of
the palate and the tissue surface of the upper dentures. For
direct microscopic examination and detection of C. albicans
hyphae, scraped specimen from the inflamed tissue of the
palate was collected by using a sterile lancet.
Microbiological procedures
Direct microscopical examination
The calcofluor white stain was used for the direct micro-
scopical examination of saliva and smear samples [28]. The
slides were examined with a fluorescent microscope
(Olympus BH2-RFCA, Japan) for the detection of hyphae
and budding yeast cells.
Culture procedures
Saliva samples were mixed well, and 1 ml was inoculated
onto Sabouraud dextrose agar (SDA) supplemented with
364 Clin Oral Invest (2009) 13:363–368
chloramphenicol (50 mg/l) and penicillin (50 mg/l) for
isolation of yeasts. For the isolation of Lactobacillus
species, one loop (0.01 μl) of the same sample was plated
onto Rogosa agar [52]. Swab samples were plated directly
on SDA and Rogosa agar. SDA plates were incubated at
37°C in aerobic conditions for 24 h. Rogosa agar plates
were incubated at 37°C in anaerobic conditions for 24 h
[22,52].
Identification of yeast species
The yeasts grown from saliva were expressed as colony
forming units per milliliter (cfu/ml). The number of yeast
colonies grown from swab specimens was evaluated as
follows:
1. Light growth: Colonies are seen only at the first part of
the agar plate.
2. Medium growth: Colonies are seen at the first and
second part of the agar plate.
3. Heavy growth: Colonies are seen at the first, second,
and third part of the agar plate.
4. Very heavy growth: Colonies are seen at all parts of the
agar plate.
Morphologically, different colonies were picked and
reinoculated onto SDA for purity. Identification of yeast
isolates to the species level were based on standard methods
such as chlamydospore production on corn meal agar
supplemented with 1% Tween 80 and carbohydrate assimila-
tion pattern by using the API ID 32°C (Biomerieux, Marcy
I’Etoile, France). In addition, growth at 45°C, colony
morphology, and chlamydoconidia production on Staib agar
were used for discriminating C. albicans and Candida
dubliniensis.C. albicans ATCC 10231 and C. dubliniensis
CD36I were used as control strains [22].
Identification of Lactobacillus species
Rogosa agar was used as a selective media for the isolation
of Lactobacillus species. All different colonies grown on
Rogosa agar plates were examined by Gram stain. Gram-
positive Bacillus strains were replated into lactobacilli MRS
broth tubes supplemented with glucose, maltose, mannitole,
or saccharose. Growth in this broth and esculin hydrolysis
was used for identification [52].
Whitney–Mann Uand Chi-square tests were used for
statistical analysis of the results.
Fig. 1 Hyphae from a patient’s smear sample (×200, prepared with
calcofluor white)
Fig. 2 Hyphae and yeast cells from a patient’s smear sample (×400,
prepared with calcofluor white)
Table 1 The differences of the patient age, denture age, and Candida
albicans counts in saliva, candidal growth on the palate and the tissue
surface of the denture base, hyphae growth in saliva, on the palate, and
continuous denture wearing habit between the patients with and without
DRS is shown
Patients p
With DRS
(n=71)
Without
DRS
(n=20)
Patient age (year) 62.17± 9.4 69.95± 9.8 0.006
Denture age (year) 9.5± 8.2 4.7± 6.6 0.003
Candida count in saliva
(cfu/ml)
2,281.6±
3,803.6
305.3±
674.9
0.001
Candida growth in palate (%) 66.2 25 0.002
Candida growth in denture (%) 81.7 30 0.000
Hyphea growth in saliva (%) 95 5 0.001
Hyphea growth in palate (%) 100 0 0.001
Lactobacillus growth in saliva
(%)
87.3 65 0.028
Continuous denture wearing
(%)
85.9 60 0.015
Clin Oral Invest (2009) 13:363–368 365
Results
The microscopic images of C. albicans hyphae and yeast
cells from a patient’s smear sample were shown in Figs. 1
and 2.
The differences of the patient age, denture age, and C.
albicans counts in saliva, candidal growth on the palate and
the tissue surface of the denture base, C. albicans hyphae
growth in saliva, on the palate, and continuous denture
wearing habit between the patients with and without DRS
were shown in Table 1. Chi-square and Mann–Whitney U
tests were used to analyze the differences.
The subjects in which C. albicans hyphae were observed
in their saliva and on the palate were analyzed for the C.
albicans counts using Mann–Whitney Utest and for the
Lactobacillus growth using Chi-square test (Table 2). The
C. albicans counts were found statistically significant
higher in the subjects with hyphae in their saliva or on
the palate, compared to the subjects without hyphae.
However, Lactobacillus growth was found statistically
higher only in subjects with C. albicans hyphae in their
saliva. For the subjects with C. albicans hyphae growth on
the palate, there was no statistically significant difference.
Although there was a noticeable increase in C. albicans
counts in saliva due to the clinical intensity (Newton
classification) of DRS, no statistical significant differences
were found. In patients with papillary hyperplasia (Newton
type 3), the Lactobacillus incidence was higher on the palate;
however, this difference was also not supported statistically
(Table 3).
Discussion
C. albicans is the most common type of microorganism
found in oral candidal infections [17,51]. The higher
prevalence of C. albicans was explained by the higher
capability to adhere to mucosal surfaces, which is considered
as the first step in the pathogenesis of oral candidiasis [19].
The results of the present study indicate that C. albicans
counts are higher in patients with DRS compared with the
healthy group of patients. The high capability of Candida
species to adhere to mucosal surfaces is reported to be
enhanced especially by the transition from blastospores to
hyphae [2], which is a striking feature of C. albicans biology.
This property of C. albicans could promote tissue penetra-
tion during the early stages of infection [48]. In healthy
environment, the host’s defense systems must be preventing
theinfection.Thereissomeevidencethatoralepithelial
cells may present a topical defense response to Candida
[34]. As Budtz-Jorgensen et al. had pointed out to the
importance of C. albicans hyphae in DRS [8], in this
study, the presence of hyphae seemed to facilitate the C.
albicans colonization.
It was suggested that the denture plaque on tissue
surfaces of dentures must have an irritating effect on the
mucosa [5,12,14,23]. Denture plaque is composed of
many different microorganisms, particularly of bacteria and
C. albicans [11,13,42]. Lactobacillus counts, as well as
the presence of yeasts in saliva, were found to be associated
with the secretion rate of saliva [44]. Salivary components
and the cleansing action of the tongue are a part of the hosts
Table 2 The effect of hyphae presence on Candida albicans count and Lactobacillus growth is shown
Hyphae
In saliva On the palate
Presence (n=24) Absence (n=67) pPresence (n= 13) Absence (n=78) p
Mean SD Mean SD Mean SD Mean SD
Candida albicans count (cfu/ml) 5,308.5 5,184.7 607.4 1,055.8 0.001 6,959.6 6,011.4 995.2 1,810.1 0.001
Lactobacillus growth (%) 95.8 77.6 0.036 92.3 78.2 0.218
Table 3 The relation between clinical intensity and Lactobacillus growth and Candida albicans counts is shown
Clinical intensity of DRS
Newton 1 (n=30) Newton 2 (n=27) Newton 3 (n=14)
Mean SD Mean SD Mean SD
Candida albicans count (cfu/ml) 1,578,700 2,717,119 2,374,037 4,677,758 3,609,429 3,822,830
Lactobacillus growth (%) 86.7 85.2 92.9
366 Clin Oral Invest (2009) 13:363–368
defense balance. The isolation of oral tissues under a
denture, especially a large area under a complete maxillary
denture that seals and forms its own microenvironment,
represents a local alteration that disturbs the normal balance
[45]. In addition to the duration dentures are worn, it was
suggested that DRS is associated with the amount of tissue
covered by a denture. DRS prevalence was found to be
higher in complete maxillary denture cases [37,33,36,40,
46,51]. Reduced salivary flow and dependant simultaneous
changes in protein content, electrolyte content, buffering
capacity, antibodies, and nonspecific antimicrobials of
whole saliva are considered to be the main causes of the
frequently detected rapid development of post-radiation
caries and the quantitative and qualitative shifts in oral
microflora. These patients are reported to be at high risk
for rampant dental caries because of the loss of buffering
capacity in their saliva and a shift in the microbial
flora favoring an increase in Streptococcus mutans and
lactobacilli [4,15].
The toxic effects of plaque masses in contact with oral
mucosa for extended periods of time are predictable and
similar as in the periodontal patient. Continuous denture
wearing could be an attribute, strengthening this effect [47]
as observed in our study, too. Individuals wearing their
complete dentures 24 h a day were reported to show more
DRS [20,24,47]. Due to the deterioration of the dentures
in time, such as the polished surfaces fit to the underlying
tissues and the occlusion, dentures could become more
irritant to the mucosa and more open to candidal and
bacterial colonization [6]. In this manner, the results of this
present study showed a statistically significant relation
between denture age and C. albicans counts.
C. albicans does not necessarily cause disease; there
have to be some other predisposing factors [39]. The most
important result of this study was that it showed the
importance of C. albicans hyphae in the development of
DRS. The presence of hyphae seems to facilitate the candidal
colonization on the mucosal surfaces and raising the C.
albicans counts.
The results of this study indicated an association between
Lactobacillus counts and C. albicans hyphae incidence.
The explanation of this positive correlation might be the
above-mentioned relation between oral hygiene and micro-
organism growth. Poor oral hygiene and the covered palate
might enhance both the Lactobacillus and C. albicans
hyphae growth in the oral cavity because of the missing
rinsing action of saliva. Although our results showed no
statistically significant association between continuous
denture wearing and microorganism growth, this factor
should be further investigated in higher patient numbers to
draw conclusions.
Epidemiological facts about DRS, such as gender, age of
patients, and the type and localization of dentures, are
factors which are not possible to manipulate, whereas
motivation of the patient not to wear the dentures at night
and renewing the dentures in reasonable time intervals
would be an easy measure to reduce the prevalence of
DRS dramatically. It would be of importance to concen-
trate on patient information and motivation on hygiene for
prophylactic purposes.
Conclusions
1. C. albicans must be an important factor in the
formation of denture-related stomatitis since its counts
in DRS patients are statistically higher than in healthy
subjects.
2. Hyphae seem to facilitate the rise of C. albicans counts
and be related to the inflammatory response of the tissues.
3. Lactobacillus seems to play an important role in the
presence of DRS as well.
4. In agreement with many other studies, the results of
this study confirm the importance of denture age and
continuous denture wearing in the development of
DRS.
Conflict of interest The authors declare that they have no conflict of
interest.
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