Denture stomatitis and salivary vascular

endothelial growth factor in immediate

complete denture wearers with type 2
diabetes
Katarina Radovi
c, DMD, MDS,a Jugoslav Ili
c, DMD, PhD,b
Jelena Roganovi
c, DMD, PhD,c Dragica Stoji
c, DMD, PhD,d
Bozidar Brkovi
c, DMD, PhD,e and Georgina Pudar, DMD, PhDf
School of Dental Medicine, University of Belgrade, Belgrade, Serbia;
University Medical Center Zvezdara, Belgrade, Serbia
Statement of problem. Diabetes mellitus type 2 is associated with a variety of oral mucosal changes, including an altered level
of salivary vascular endothelial growth factor. However, the authors identified no studies concerning denture stomatitis and
salivary vascular endothelial growth factor in immediate denture wearers with diabetes mellitus type 2.

Purpose. The purpose of this study was to investigate the incidence of and risk factors for denture stomatitis in immediate
complete denture wearers with and without diabetes mellitus type 2 and to investigate the relationship between levels of
salivary vascular endothelial growth factor and clinical forms of denture stomatitis in both groups.

Material and methods. Individuals without diabetes (n¼42) or with diabetes mellitus type 2 (n¼36) who were candidates for
complete immediate dentures were included in the study. After 1 year of wearing relined immediate dentures, participants
were evaluated for denture stomatitis and potential contributing factors. Salivary vascular endothelial growth factor levels
were measured with enzyme-linked immunosorbent assays. Data were analyzed with the c2 test or the Student t test where
appropriate, as well as with binary logistic regression analysis.

Results. The incidence of denture stomatitis was 61% in participants with diabetes mellitus type 2 and 38% in those without
diabetes. Low denture stability and diabetes mellitus type 2 were risk factors for denture stomatitis. Salivary vascular
endothelial growth factor concentrations at the beginning of the study were 557.6 94.7 pg/mL in participants with diabetes
mellitus type 2 and 103.5 21.6 pg/mL in those without diabetes. In Newton Type I and Newton Type II denture stomatitis,
vascular endothelial growth factor levels were 460.9 55.4 pg/mL and 1445.2 422.1 pg/mL in individuals with diabetes
and 73.2 10.0 pg/mL and 306.5 22.6 pg/mL in those without diabetes.

Conclusions. Perceived denture stability and diabetes mellitus type 2 are independent risk factors for the occurrence of
denture stomatitis. Altered salivary vascular endothelial growth factor levels and denture stomatitis are more prevalent in
denture wearers with diabetes mellitus type 2. (J Prosthet Dent 2014;111:373-379)

Clinical Implications
Wearers of immediate complete dentures, especially those with diabetes
mellitus type 2, require special attention regarding denture stability.
Results indicate alterations in the salivary vascular endothelial growth
factor levels of denture wearers with type 2 diabetes and suggest that the
modulation of vascular endothelial growth factor activity could be a
useful therapeutic approach to regulating oral complications such as
denture stomatitis in those with diabetes mellitus type 2.

This study was supported by the Serbian Ministry of Education and Science, Grant No. 175021.
a
Lecturer, Department of Prosthodontics, School of Dental Medicine, University of Belgrade.
b
Lecturer, Department of Restorative Odontology and Endodontics, School of Dental Medicine, University of Belgrade.
c
Lecturer, Department of Pharmacology in Dentistry, School of Dental Medicine, University of Belgrade.
d
Professor, Department of Pharmacology in Dentistry, School of Dental Medicine, University of Belgrade.
e
Assistant Professor, Department of Oral Surgery, School of Dental Medicine, University of Belgrade.
f
Professor, Department of Endocrinology, Diabetes and Metabolic Diseases, University Medical Center Zvezdara, Belgrade.

Radovi
c et al
374
Diabetes mellitus is commonly found
in dental patients.1 The common oral
disturbances associated with diabetes
mellitus include periodontal disease,
salivary gland dysfunction, burning
mouth, delayed healing of oral wounds,
and various types of stomatitis, in-
cluding denture stomatitis.2-6
Diabetes mellitus is a disease with
serious systemic complications, and
extensive clinical efforts have been made
to improve the quality of life of patients
with diabetes. Given that a well-
balanced diet is a component of dia-
betes therapy, the rational therapeutic
option for future complete denture
wearers, who are also candidates for
preprosthetic extraction procedures,
could be to receive immediate dentures
on the day of extractions.7 In denture
wearing, the oral mucosa must be able
to mechanically and physiologically
resist the persistent pressure required for
denture support and movement during
function.8 Incorrect vertical dimension
and denture instability may contribute
to the occurrence of denture stomati-
tis.9,10 Although studies have found a
prevalence of denture stomatitis among
complete denture wearers,10-12 infor-
mation is lacking as to immediate den-
ture wearers with diabetes mellitus
type 2.
Vascular endothelial growth factor
(VEGF) is a potent cytokine produced by
many types of cells and functions as a
major regulator of physiologic and
pathologic angiogenesis.13,14 This factor
may be one of the underlying markers of
chronic inflammatory or autoimmune
conditions in the oral cavity.15-18 The
level of VEGF in human saliva derived
from the secretions of the major and
minor salivary glands19,20 is elevated in
patients with diabetes.21
The objective of this study was to
determine the frequency of and risk fac-
tors for denture stomatitis in immedi-
ate complete denture wearers with
and without diabetes mellitus type 2.
Because salivary VEGF may be involved
in the maintenance of oral mucosa ho-
meostasis, and because its connection
with denture stomatitis has not yet been
reported, the salivary levels of VEGF
The Journal of Prosthetic Dentistry
were also determined in different types
of denture stomatitis in individuals with
and without diabetes. The null hypoth-
eses were that diabetes mellitus type 2 is
not associated with denture stomatitis
and that the level of salivary VEGF is not
changed in denture stomatitis.
MATERIAL AND METHODS
Study population
The study population comprised 78
participants aged 45 to 64 years. Forty-
two participants with diagnosed dia-
betes mellitus type 2 were recruited
from the Zvezdara University Medical
Center, Belgrade, and 42 participants
without diabetes were recruited from
the Department of Prosthodontics,
School of Dental Medicine, University
of Belgrade. The inclusion criteria were
wearing maxillary partial removable
dental prostheses and mandibular
complete dentures for approximately
10 years; the presence of 3 teeth with
signs of terminal periodontitis in the
anterior and premolar maxillary re-
gions; the absence of any lesions in the
oral cavity; and, for participants with
diabetes, a disease history of at least 2
years with a glycosylated hemoglobin
measurement less than 9 (HbA1c<9).
The exclusion criteria were smoking; not
wearing new dentures on a regular basis
in the previous 12 months; and using
adhesive pastes, powders, or pads. Six
individuals from the diabetes mellitus
type 2 group were excluded because
they had not regularly worn new den-
tures and had used adhesives; the final
number of participants with diabetes
mellitus type 2 was 36.
Preprosthetic procedures included
verifying the absence of lesions in the oral
cavity, giving oral hygiene instructions,
and performing nonsurgical extractions
of the remaining 3 maxillary teeth.
Maxillary immediate complete dentures
were indicated for participants both with
and without diabetes to provide partic-
ipants with diabetes mellitus type 2 with
adequate mastication and to stan-
dardize the study conditions. Also, the
existing mandibular complete dentures
Volume 111 Issue 5
were replaced on the day of receiving
maxillary immediate complete dentures
with a balanced occlusal scheme. The
fabrication of new dentures (maxillary
immediate complete dentures and
mandibular complete dentures) was
performed at the Department of Pros-
thodontics, School of Dental Medicine,
University of Belgrade. The study proto-
col was approved by the Ethics Com-
mittee of the Faculty of Dentistry,
University of Belgrade (No. 32/36), and
the study was conducted in accordance
with the Helsinki Declaration.
Clinical examinations
Dental records for all participants
were provided at the Department of
Prosthodontics and Clinic of Oral Sur-
gery, School of Dental Medicine, Uni-
versity of Belgrade. Regular follow-up of
the postextraction wound healing pro-
cess for participants with an immediate
denture was scheduled weekly for 3
weeks. During that time, prosthetic
evaluation was performed, consisting of
postinsertion denture adjustments to
address pain and discomfort and to
improve masticatory ability, denture
stability, and occlusion. During the 3-
month period after denture insertion, if
participants reported decreased denture
retention and stability, the prostheses
were relined with acrylic hard reline resin
material (Simgal R; Galenika).
The presence of denture stomatitis
and potential contributing factors, such
as denture cleanliness and stability, were
evaluated 1 year after the immediate
denture insertion. Two independent,
calibrated examiners performed oral ex-
aminations and diagnosed denture sto-
matitis according to the Newton
classification,22 that is, Newton Type I
(pinpoint hyperemia with small areas of
inflammation in an otherwise normal
tissue); Newton Type II (diffuse hyper-
emia characterized by generalized
inflammation of the entire denture-
bearing area and a smooth mucosal
surface and in which slight trauma may
be sufficient to cause bleeding); and
Newton Type III (granular mucosa with a
nodular hyperemic surface, which may
Radovi
c et al
May 2014
be present over the entire denture-
bearing area but is more commonly
restricted to central areas). Denture
cleanliness was assessed clinically ac-
cording to the modified Hoad-Reddick
classification,23 that is, clean (without
any soft/hard debris or stain) or dirty
(with soft and hard debris or stain after
dentures were washed under tap water).
A subjective measure of denture sta-
bility was used and expressed as
perceived denture stability, which could
be a proxy measure for trauma during
function. Satisfaction with the perceived
stability of the prosthesis was expressed
as low (movement or displacement of
dentures during mastication, talking, or
rest) or high (absence of movement or
displacement of dentures during masti-
cation, talking, or rest).
Saliva specimens were collected from
all participants before teeth extraction
and prosthetic treatment and from par-
ticipants with denture stomatitis 1 year
after denture insertion and wearing. The
mouth was rinsed with tap water before
the saliva specimen was collected. All
participants were asked to retain mixed
saliva in their mouth for 5 minutes
without swallowing and then to expec-
torate into a clean plastic container.
The specimens were frozen in liquid ni-
trogen and stored at -70 C until anal-
ysis. The saliva was thawed, centrifuged
(10 000 g, 5 minutes at 4 C) to remove
cell debris, and assayed for VEGF.
The concentrations of VEGF in saliva
(pg/mL) were measured by commer-
cially available enzyme-linked immuno-
sorbent assay (HumanVEGF ELISA Kit
for Serum, Plasma, Cell Culture Super-
natant, Urine; RayBiotech) according to
the manufacturer’s instructions. Optical
densities were measured at 450 nm
with a microplate reader, and the mini-
mum detectable level of the test was
5.0 pg/mL.
On the basis of the results from pre-
vious studies (in which the differences in
frequency of denture stomatitis between
complete denture wearers without and
with diabetes were 15%5 and 28%24), the
calculated sample size of 78 participants
was sufficient to detect a 20% difference
in prevalence between groups with a
Radovi
c et al
power of .80 and with a¼.05 (2-tailed)
with the c2 test.
The results are presented as fre-
quencies or as mean standard devia-
tion. The frequency of denture stomatitis
and potential contributing factors in the
whole population were analyzed with
the c2 test. For binary logistic regression
analyses, the odds ratios (ORs) and their
95% confidence intervals (CIs) were
calculated to determine the relation-
ships between denture stomatitis and
each potential predictor variable indi-
vidually (unadjusted test); associations
between variables that were found to be
significantly associated with denture
stomatitis were adjusted for potential
confounding effects (adjusted test). The
frequency of denture stomatitis and
potential contributing factors in partic-
ipants with and without diabetes were
analyzed with the c2 test. The Student t
test for dependent samples (before
versus 1 year after denture insertion) and
independent samples (without diabetes
versus the diabetes mellitus type 2
group) was used to analyze salivary
VEGF concentrations in Newton Type I
and Newton Type II groups. Statistical
significance was set at a¼.05. Data were
analyzed with statistical software (Stat
for Windows 8; StatSoft Inc).
RESULTS
The frequency of denture stomatitis
observed after 1 year of wearing com-
plete immediate dentures was around
49% in the entire study population
(Table I). Table I also shows the fre-
quency of potential contributing factors
for the development and severity of
denture stomatitis: denture cleanliness,
perceived stability, and presence of dia-
betes mellitus type 2. The analysis did
not include age and sex as potential
contributing factors, because the group
consisted predominantly of male par-
ticipants (69%) aged between 45 and 64
years. Low denture stability (P¼.003)
and diabetes mellitus type 2 (P¼.04)
were significantly associated with the
development of denture stomatitis. In
contrast, for denture cleanliness there
was no statistical difference between
375
participants with and without denture
stomatitis (P¼.35). Results concerning
the severity of denture stomatitis indi-
cated that Newton Type I and Newton
Type II, but not Newton Type III, were
observed in participants in this study
(Figs. 1, 2). Statistical analysis found
that denture stability (P¼.008), unlike
denture cleanliness (P¼.35) and dia-
betes mellitus type 2 (P¼.74), was
significantly associated with the severity
of denture stomatitis (Table I).
The binary logistic regression model
presented in Table II shows that the risk
for denture stomatitis development was
3.82 times greater in immediate denture
wearers who reported low stability than
in those for whom stability was high
(P<.05; OR, 3.82; 95% CI, 1.43 to
10.17). Diabetes mellitus type 2
increased the risk of denture stomatitis
2.55 times (P<.05; OR, 2.55; 95% CI,
1.02 to 6.37). An adjusted test for the
association of diabetes mellitus type 2
and low denture stability found a
decrease of the adjusted ORs in com-
parison with the unadjusted ORs (2.04
versus 2.55 for diabetes mellitus type 2
and 3.31 versus 3.82 for low denture
stability), implying that the risk for
denture stomatitis would not be poten-
tiated if both factors were involved. Low
denture stability increased the severity of
denture stomatitis 8.25 times (P<.05;
OR, 8.25; 95% CI, 1.50 to 45.42)
(Table II).
The frequency of denture stomatitis,
denture cleanliness, and perceived sta-
bility in immediate denture wearers
without diabetes and with diabetes
mellitus type 2 are presented in Table III.
The frequency of denture stomatitis in
participants with diabetes was signifi-
cantly higher than in individuals without
diabetes. Perceived stability was signifi-
cantly lower in participants with dia-
betes mellitus type 2 than in those
without diabetes, and denture cleanli-
ness did not differ statistically between
the investigated groups (Table III).
The concentration of salivary VEGF
before immediate denture insertion (un-
der the condition of wearing a partial
denture) in participants with diabetes
mellitus type 2 was significantly higher
376 Volume 111 Issue 5
Table I. Potential contributing factors for development and severity of denture stomatitis in immediate complete
denture wearers
Development of
Denture Stomatitis Severity of Denture Stomatitis
Absence Presence Newton Newton
Parameters (n[40) (n[38) P Type I (n[25) Type II (n[13) P

Denture cleanliness: dirty 20.0% (8) 28.9% (11) .35 24.0% (6) 38.5% (5) .35

Perceived stability: low 22.5% (9) 55.3% (21) .003 40.0% (10) 84.6% (11) .008
Diabetes mellitus type 2: presence 35.0% (14) 57.9% (22) .04 56.0% (14) 61.5% (8) .74

P value from c2 test.

presence or absence of diabetes mellitus

type 2 (Table IV).

DISCUSSION

Obtained data have indicated that

1 Palatal denture stomatitis, Newton Type I.
2 Palatal denture stomatitis, Newton Type II.
(P<.01) than in the group without dia-
betes (557.6 94.7 pg/mL in those with
diabetes versus 103.5 21.6 pg/mL in
those without diabetes; data not shown).
The analysis of differences in salivary
VEGF levels between participants with
and without diabetes who developed
denture stomatitis found that salivary
VEGF concentrations were significantly
The Journal of Prosthetic Dentistry
higher in the group with diabetes than in
the group without diabetes, regardless of
the type of denture stomatitis (Table IV).
Also, unlike the Newton Type I group, in
which salivary VEGF concentrations
decreased, the Newton Type II group had
increased salivary VEGF values 1 year
later, compared with measurements
before denture insertion, regardless of the
diabetes mellitus type 2 is one of the
risk factors associated with the devel-
opment of denture stomatitis and that
salivary VEGF levels are altered in den-
ture stomatitis. Therefore, the null hy-
potheses were rejected.
Approximately half of the entire
population investigated exhibited den-
ture stomatitis 1 year after the insertion
and wearing of immediate complete
dentures. In a comparison of the prev-
alence of denture stomatitis between
immediate denture wearers without
diabetes and those with diabetes mel-
litus type 2, the results indicated a
significantly higher frequency of denture
stomatitis in participants with diabetes
(around 61%) compared with those
without diabetes (around 38%).
Comparative studies concerning the
prevalence of denture stomatitis in
complete denture wearers without and
with diabetes are conflicting. For
example, the higher prevalence of
mucosal disturbances associated with
denture stomatitis in patients with
diabetes mellitus type 2 was found by
Guggenheimer et al5 and by Collin
et al,24 but not by De Lima et al.6
The advantage of an immediate
denture as a therapeutic choice for
patients with diabetes mellitus is the
possibility of immediate masticatory
function after tooth extraction,
Radovi
c et al
May 2014
Table II. Unadjusted odds ratios for potential contributing factors versus
adjusted odds ratios for risk factors predicting denture stomatitis in immediate
complete denture wearers
Variable Category OR (95% CI)
Appearance of
denture stomatitis
Diabetes mellitus type 2 Absence
Presence
Perceived stability High
Low
Denture cleanliness Clean
Dirty
Severity of denture stomatitis
Diabetes mellitus type 2
Perceived stability
Denture cleanliness
OR, odds ratio; AOR, adjusted odds ratio.
P value from c2 test.
Table III. Characteristics of immediate denture wearers with and without
diabetes mellitus type 2
Parameters
Frequency of denture stomatitis
Denture stomatitis: presence
Newton Type I: presence
Newton Type II: presence
Potential contributing
factors for denture stomatitis
Denture cleanliness: dirty
Perceived stability: low
P value from c2 test.
providing good nutritional status for
normoglycemia. The disadvantage of
such a prosthesis is the temporary lack
of retention and stability during the
postinsertion period, which is usually
corrected by relining. Obtained results
indicated significantly lower denture
stability in participants with diabetes
mellitus type 2 compared with the
group without diabetes after 1 year of
wearing relined immediate dentures.
Radovi
c et al
377
reduced saliva secretion. For example,
Collin et al24 have found an increased
incidence of dry mouth in patients with
diabetes mellitus type 2 compared with
P AOR (95% CI) P
individuals of the same age without
diabetes, owing to diabetic neuropathy
of autonomic nerves innervating the
1 salivary glands. Moreover, in addition
2.55 (1.02-6.37) .045 2.04 (0.78-5.34) .14
to the influence of saliva on denture
stability, another significant contrib-
1
uting factor of hyposalivation on the
3.82 (1.43-10.17) .007 3.31 (1.21-9.02) .019 development of denture stomatitis is
1 the promotion of irritation of the soft
1.63 (0.57-4.63) .36 tissues by hard denture materials,
which is accompanied by increased
exfoliation of epithelial cells and
mucosal ulcerations in patients with
Absence 1 diabetes.4 Based on these data, a
Presence 1.26 (0.32-4.93) .74 higher incidence of denture stomatitis
High 1 in diabetes mellitus type 2 denture
Low 8.25 (1.5-45.42) .015 wearers may be caused by impaired
denture stability and irritation due to
Clean 1
diabetes-induced hyposalivation.
Dirty 0.50 (0.12-2.14) .35
Obtained results also indicate that
diabetes mellitus type 2 and perceived
stability are independent risk factors for
the development of denture stomatitis
in immediate denture wearers. Howev-
er, binary logistic regression analysis
after adjustment found the lack of
Nondiabetic Diabetes Mellitus
potentiation between mentioned vari-
(n[42) Type 2 (n[36) P ables. In connection with this, the lim-
itations of this study should be
mentioned. Given that the number of
38.1% (16) 61.1% (22) .04
predictor variables was relatively small
26.2% (11) 38.9% (14) .23 and that all variables were qualitative,
11.9% (5) 22.2% (8) .33 additional clinical factors should be
introduced into the analysis to better
predict denture stomatitis in immediate
19.0% (8) 30.5% (11) .23 denture wearers, and further investiga-
tion is necessary.
26.2% (11) 52.8% (19) .04
VEGF mRNA and protein are
expressed constitutively in normal hu-
man salivary acinar cells, and VEGF is
The relevance of the contribution of secreted in saliva in concentrations suf-
saliva for complete denture retention is ficient to be angiogenic.19,20 In chroni-
well established and is due to its vis- cally inflamed glands, considerable
cosity and surface tension and the amounts of VEGF are found in both
maintenance of a good peripheral glandular epithelium and inflammatory
seal.25,26 Although all participants in cells.19 The present results indicate that
this study, without diabetes and with salivary VEGF concentrations before
diabetes mellitus type 2, belong to an immediate denture insertion are signifi-
older population characterized by sub- cantly higher in participants with dia-
jective and objective xerostomia,27 pa- betes mellitus type 2 than in those
tients with diabetes express significantly without diabetes. This agrees with the
378
Table IV. Salivary vascular endothelial growth factor concentrations in partici-
pants with and without diabetes mellitus type 2 before denture insertion and with
denture stomatitis (Newton Type I or II) observed 1 year after denture insertion
Saliva Collection Time
Newton Type I
Before denture insertion
One year after denture insertion
P**
Newton Type II
Before denture insertion
One year after denture insertion
P**
*Student t test for independent samples.
**Student t test for dependent samples.
findings of Surdacka et al,21 who found
increased salivary VEGF in pregnant
women with diabetes compared with
pregnant women without diabetes.
Detected changes of salivary VEGF levels
after different types of denture stomati-
tis are more pronounced in partici-
pants with diabetes mellitus type 2
than in participants without diabetes.
Decreased levels of VEGF in Newton
Type I and increased levels in Newton
Type II were detected, with respect to
baseline values in both participants with
diabetes mellitus type 2 and those
without diabetes. The decreased levels of
salivary VEGF in Newton Type I denture
stomatitis may be the result of pre-
prosthetic tooth extractions that elimi-
nated periodontal inflammation, which
is characterized by increased salivary
VEGF,15,16 and of low-grade oral
mucosal inflammation in Newton Type I
denture stomatitis. As Newton Type II
is characterized by a higher level of
mucosal inflammation than Newton
Type I, and although VEGF tissue levels
were not measured, the inflammatory
cells of the oral lesions releasing VEGF
may contribute to the elevated levels of
VEGF in whole saliva in Newton Type II
denture stomatitis. In addition to sali-
vary gland tissue, other sources
contribute to the salivary VEGF pool,
such as the VEGF produced by the oral
The Journal of Prosthetic Dentistry
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379
Corresponding author:
Dr Dragica Stoji
c
Department of Pharmacology in Dentistry
School of Dental Medicine
University of Belgrade
Dr Subotica 8, Belgrade
SERBIA
E-mail: dragica.stojic@stomf.bg.ac.rs
Acknowledgments
The authors thank Ms. Dusica Djukic for lan-
guage editing and Mr. Dubravko Bokonjic for
supervision of statistical processing of data.
Copyright ª 2014 by the Editorial Council for
The Journal of Prosthetic Dentistry.

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