Download Oral hygiene and periodontal treatment needs in children and

A. Tsami*, P. Petropoulou*, J. Panayiotou**,
Z. Mantzavinos*, E. Roma-Giannikou**
*Department of Periodontology, Dental School, Athens University,
Athens-Greece
**First Department of Paediatrics, Athens University, Athens-Greece
e-mail: [email protected]
Oral hygiene and
periodontal treatment
needs in children and
adolescents with coeliac
disease in Greece
ABSTRACT
Aim To evaluate the factors that influence the oral hygiene
and the periodontal treatment needs of children and
adolescents with coeliac disease (CD) in Greece.
M e t h o d s The sample consisted of 35 children and
adolescents, aged 4-18 years. The evaluation included
consideration of the detailed medical history, the duration
of CD and of gluten-free diet, the history of oral mucosal
findings and a dental questionnaire that included
information about oral hygiene habits, symptoms of
periodontal disease and dental attendance. The clinical
dental examination consisted of the simplified gingival
index, the oral hygiene index and the periodontal
screening and recording index.
Statistics The chi square and logistic regression analysis
were performed in order to determine the factors or
parameters that had a statistically significant (p< or =0.05)
impact on oral hygiene and periodontal treatment needs
of children and adolescents with CD.
Results The periodontal treatment need of children and
adolescents with CD were high and most of them needed
treatment of gingivitis (60.01%) and only a few subjects
had a healthy periodontium (34.29%). The periodontal
treatment need index, the simplified gingival index and the
hygiene index correlated statistically significantly with the
presence of a coexisting disease, frequency of tooth
brushing, bleeding upon brushing and oral malodor.
Conclusion The periodontal treatment need of children
and adolescents with CD correlated with factors that
related to the presence of a second medical condition and
to the personal oral hygiene habits. Additionally, the oral
hygiene level and periodontal status of children with CD
do not have any specific characteristics but they have
similarities to the oral hygiene level and periodontal status
of the children of the general population.
Keywords: coeliac disease, periodontal treatment,
oral hygiene, children, adolescents.
122
Introduction
Coeliac disease (CD) is an autoimmune chronic disorder
characterised by permanent intolerance, mediated by Tlymphocytes, to the polypeptide fragments of gluten a
protein found in wheat, rye and barley. This disease is
characterised by a total or sub-total villous atrophy of the
proximal intestine, resulting in poor absorption of the
majority of nutrients and vitamins [Schuppan, 2000; Colin
and Reunala, 2003; Seyhan et al., 2007].
The aetiology of CD is not fully understood, but there is
a clinical and histological improvement on a strict glutenfree diet and relapse when dietary gluten is reintroduced
[Schuppan, 2000; Poon and Nixon, 2001; Colin and
Reunala, 2003; Seyhan et al., 2007].
The classical clinical symptoms of CD include chronic
diarrhea, vomiting, irritability, anorexia, weight loss,
growth deficit, abdominal pain and distension, variable
degrees of compromised nutritional status, iron-deficiency
anemia pallor and gluteal muscle atrophy [Pastone et al.,
2008a]. The classical symptoms of CD generally can be
manifested from the sixth month of life, coinciding with
the introduction of cereals into the diet and usually occur
in children under the age of two. However, nowadays the
typical CD presentation is less frequent and many CD
patients show atypical symptoms such as abdominal pain,
vomiting or constipation as well as a number of extraintestinal problems like iron deficiency, altered bone
metabolism, short stature and unexplained elevation of
transaminases or show minimal symptoms or are even
asymptomatic [Roma et al., in press].
The prevalence of CD in Europe and USA in children
between 2.5 and 15 years of age is approximately 1:300 to
1:85, varies from country to country and predominantly
affects white individuals and children, who tend to have
more severe symptoms often leading to growth retardation,
malnutrition and significant weight loss and osteoporosis
[Cataldo and Montalto, 2007; Torres et al., 2007].
Several authors have described a greater prevalence of
some oral manifestations in CD patients, which are tooth
enamel defects such as hypoplasia, recurrent oral aphthous
stomatitis and pain or burning of the tongue [Aine, 1996;
Poon and Nixon, 2001; Priovolou et al., 2004; Farmakis et
al., 2005; Bucci et al., 2007; Bossù et al., 2007; de Lima et
al., 2008; Pastone et al., 2008b]. These oral manifestations
are of fundamental importance as diagnostic aids for the
CD, especially in the coeliac forms difficult to be identified
such as the atypical or the asymptomatic forms [Aine, 1996;
Bucci et al., 2007; Pastone et al., 2008a].
In studies of patients with CD there are findings of
lesions in the gingival tissues, which are characterized as
gingivitis, similar to the one found in patients with Crohn’s
disease and which is due to the co-existence of diabetes
[Tyldesley, 1983]. Additionally, there are patients with CD
which demonstrate lichen planus [Scully et al., 1993]
ulcerative gingival lesions [Eisen, 2002; Campisi et al.,
2008] and ulcerative gingival lesions of vulvovaginal
gingival syndrome (VVGS) [Eisen, 1994; de Lima et al.,
2008]. These oral lesions may be poorly symptomatic or
may co-exist with pain, burning, discomfort and bleeding
on brushing teeth [de Lima et al., 2008]. Up-to-date, as far
as we are aware, there are no references in the literature
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ORAL HYGIENE AND PERIODONTAL NEEDS IN GREEK COELIAC CHILDREN AND ADOLESCENTS
Characteristics
Duration of CD and of gluten-free diet
Last 6 months
6-12 months
> 12 months
Type 1 diabetes mellitus
Autoimmune thyroid disease
History of oral mucosal findings
Individual
(N)
Individual
(%)
5
20
10
6
3
2
14.28%
57.14%
28.58%
17.14%
8.57%
5.71%
TABLE 1 - Duration of CD and the accompanied diseases.
concerning the presence of periodontal disease and the
treatment needs of children and teenagers with CD.
The purpose of the present study was to evaluate the
factors that influence oral hygiene and periodontal
treatment needs in children and adolescents with CD for
the first time in Greece.
Materials and methods
Study population
The study comprised 35 children and adolescents aged
4-18 years with CD, who were referred to the Department
of Periodontics from the Gastroenterology Unit of 1st
Department of Paediatrics of Athens University following
approval of the local ethical committee. Children with CD
aged less than 4 years were excluded. The diagnosis of CD
was established according to the revised criteria proposed
by the European Society of Paediatric Gastroenterology,
Hepatology and Nutrition [ESPGHN, 1990]. The diagnosis
of CD was based on the:
• presence of serum anti-tTG and/or anti-endomysium
(EmA) antibodies;
• clinical symptoms and positive histological evidence of
villous atrophy with crypt hyperplasia and increase in
intraepithelial lymphocytes on the gluten-containing
diet;
• disappearance of the symptoms and normalization of
serum anti-tTG and/or EmA on a gluten-free diet (GFD)
[ESPGHN, 1990].
All children and adolescents after CD diagnosis were
introduced to a gluten-free diet resulting in clinical remission and return of serum serology to normal. During this
phase they underwent an intra-oral examination of the
periodontal tissues.
Medical records
Medical information was obtained from children,
adolescents and their parents who positively responded to
the clinical examination. Also, information was obtained
from the hospital medical records. Especially, we selected
information regarding: the duration of CD and of the
gluten-free diet, the presence of type 1 diabetes mellitus
and autoimmune thyroid disease and the history of oral
mucocutaneous manifestations, such as geographic or
fissured tongue, recurrent aphthous stomatitis and cheilitis.
Dental questionnaire
The questionnaire was completed by the investigators (AT,
PP). The questions addressed were regarding: the frequency
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of tooth brushing, the method of tooth brushing and the
source of information about the oral hygiene needs, the
frequency of dental attendance and its reasoning and the
symptoms of periodontal disease and especially gum
bleeding on tooth brushing and oral malodor.
Clinical examination
The children and adolescents were examined at the
Department of Periodontics of the Dental School of
Athens, Greece. During the clinical examination the
following parameters were evaluated:
• Hygiene index [Lindhe, 1981] in order to record the
tooth surfaces which were free of dental plaque.
• Simplified gingival index [Lindhe, 1981] in order to
record the gingival units that presented bleeding on
probing.
• The number of examined deciduous or permanent
teeth which were fully erupted.
• Periodontal Screening and Recording [PSR-American
Academy of Periodontology, 1992] in order to define
every individual’s periodontal treatment needs within
the study population group. All clinical findings were
evaluated with the periodontal probe WHO. According
to this index, clinical findings were scored from 0, i.e.
no bleeding, calculus or defective margins and the
gingivae are healthy, to 4, i.e. probing depth greater
than 5.5 mm in at least one site of each sextant.
The clinical examination of the hygiene index and the
simplified gingival index was performed by one examiner
(PP) and the examination of the periodontal screening and
recording was performed by another examiner (AT), who
also helped the patients to complete their questionnaire.
For the intra-examiner reliability tests were performed
prior to the study and showed Kappa-scores greater than
0.8 for each of two examiners.
Statistical analysis
The mean value of each index was calculated for each
subject and the averages of the indices were analysed in Table
1. The findings from the medical records and the
questionnaires were evaluated using χ2 and logistic regression
analysis and definition of the correlation coefficient (r). The
level of significance was evaluated at p 0.05.
Results
Among the 35 individuals included in the study, 12 were
boys and 23 girls with a mean age of 10.46 (SD ± 4.33)
years and an age range 4 to 18 years. The duration of
gluten-free diet and the accompanied diseases of the
participants, according to the medical records, are shown
on Table 1. The mean hygiene index was 48.21%
(SD±15.51) and the simplified gingival index 48.82%
(SD±23.16). On the periodontal screening only 34.29% of
the children and adolescents had clinically healthy
periodontium, while in the rest different degrees of
periodontal treatment needs were identified (Table 2).
The presence of co-existing diseases such as type 1
diabetes mellitus and autoimmune thyroid disease were the
only parameters that significantly correlated with the
presence of gingival inflammation (r=0.542 p<0.01), the
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TSAMI A. ET AL.
Periodontal condition
Clinically healthy periodontium
(PSR-Code 0)
Gingivitis without calculus or other
predisposing factors (PSR-Code 1)
Gingivitis with calculus or other
predisposing factors (PSR-Code 2)
Localized shallow periodontal
pockets (PSR-Code 3)
Individual
(N)
Individual
(%)
12
34.29%
10
28.57%
11
31.44%
2
5.70%
TABLE 2 - Clinical findings on periodontal screening and
recording (PSR).
effectiveness of removing dental plaque (r=0.461 p<0.01),
and the need for periodontal therapy, as indicated by the
periodontal screening and the record index (r=0.332 p<0.05)
(Table 3).
Among the factors concerning the personal oral hygiene
habits of the 35 children and adolescents with CD it was
found that the frequency of tooth brushing was significantly
correlated with the simplified gingival index (r=0.422
p<0.01), the hygiene index (r=0.468 p<0.01) and the
periodontal screening and record index (r=0.357 p<0.05). In
addition, the source of information about the oral hygiene
needs was statistically significantly related with the
periodontal screening and record index (r=0.329 p<0.05)
(Table 4). Regarding the clinical findings from the periodontal
examination the parameters showed that the mean value of
simplified gingival index was significantly correlated with the
mean value of the hygiene index (r=0.766 p<0.01), the
periodontal screening and record index (r=0.888 p<0.01) as
Parameters
Frequency of
tooth brushing
Method of
tooth brushing
Source of information for
the oral hygiene needs
Frequency and the
reason of dental visits
Bleeding of gums
on tooth brushing
Malodor - halitosis
Gingival Index
Hygiene index
PSR
Simplified
gingival
Index
Hygiene
Index
PSR
Correlation
coefficient (r)
Correlation
coefficient (r)
Correlation
coefficient (r)
0.422**
0.468**
0.357*
0.058
0.268
0.144
0.273
0.091
0.329*
0.056
0.093
0.068
0.674**
0.684**
0.766**
0.888**
0.692**
0.736**
0.766**
0.726**
0.688**
0.682**
0.888**
0.726**
-
* p<0.05
** p<0.01
TABLE 4 - Logistic regression analysis for factors related to the
personal oral hygiene habits, symptoms and signs of
periodontal disease of 35 children and adolescents that
influence the simplified gingival index (S-GI), hygiene index (HI)
and periodontal screening and recording (PSR) .
124
Parameters
Age
Sex
Socioeconomic status
Duration of CD
Co-existing disease
* p<0.05
** p<0.01
Simplified
gingival
Index
Hygiene
Index
PSR
Correlation
coefficient (r)
0.119
0.149
0.199
0.258
0.542**
Correlation
coefficient (r)
0.017
0.215
0.153
0.187
0.461**
Correlation
coefficient (r)
0.166
0.159
0.161
0.211
0.332*
TABLE 3 - Logistic regression analysis for factors related to
profile of 35 children and adolescents and parameters that
influence the simplified gingival index (S-GI), hygiene index (HI),
periodontal screening and recording (PSR).
well as the mean value of the hygiene index with the
periodontal screening and record index (r=0.726 p<0.01)
(Table 4). Referring to symptoms of the periodontal disease
it was found that the bleeding on tooth brushing was
statistically significantly related with the simplified gingival
index (r=0.674 p<0.01), the mean value of the hygiene index
(r=0.692 p<0.01) and the periodontal screening and record
index (r=0.688 p<0.01), as was the case of the oral malodor
– halitosis with the above indexes (r=0.684 p<0.01,
r=0.736 p<0.01 and r=0.682 p<0.01 respectively) (Table 4).
Table 5 shows the personal oral hygiene conditions of 35
children and adolescents. The distribution of periodontal
treatment needs, using the X2 method and contingency
tables, revealed that the 15 subjects whose personal oral
hygiene was daily tooth brushing had less and different
kind of periodontal treatment needs from the group of 20
subjects who rarely performed tooth brushing habits.
Most of the subjects with daily tooth brushing had
recording codes of 0 and 1 of the PSR index (16 of the 20
subjects), while the subjects with rare tooth brushing had
scores of 1 and 2 of the PSR index (12 of the 15 subjects).
The difference in the distribution of periodontal treatment
needs relating to tooth brushing frequency was statistically
significant (X2=9.51 p<0.05). The 12 subjects who
referred bleeding upon tooth brushing had less and
different kind of periodontal treatment needs than the
group of 23 subjects who did not bleed upon tooth
brushing. Most of the subjects with bleeding upon
brushing had recording codes of 1 and 2 of the PSR index
(10 of 12 subjects) while the subjects without bleeding on
tooth brushing had recording codes of 0 and 1 of the PSR
index (17 of the 23 subjects). The difference in the
distribution of periodontal treatment needs related to
bleeding upon toothbrushing was not statistically
significant (X2=7.55 p>0.05). In addition, 9 subjects with
oral malodor had less and different kind of periodontal
treatment needs than the group of 26 subjects who did
not have oral malodor. Most of subjects with oral malodor
had recording codes of 1 and 2 of the PSR index (7 of the
9 subjects) while the subjects without oral malodor had as
recording codes of 0 and 1 of the PSR index (18 of the 26
subjects). The difference in the distribution of periodontal
treatment needs related to oral malodor was not
statistically significant (X2=4.60 p>0.05).
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Oral
hygiene
conditions
Code 0
Frequency of tooth brushing
Daily
2
(5.71%)
Rarely
10
(28.58%)
Bleeding on tooth brushing
Yes
1
(2.85%)
11
(31.44%)
Malodor halitosis
Yes
1
(2.85%)
No
11
(31.44%)
Code 1
Code 2
Code 3
Total
χ2 Level of
significance
4
(11.44%)
6
(17.15%)
8
(22.85%)
3
(8.58%)
1
(2.85%)
1
(2.85%)
15
(42.85%)
20
(57.15%)
9.51
4
(11.44%)
6
(17.15%)
6
(17.15%)
5
(14.28%)
1
(2.85%)
1
(2.85%)
12
(34.29%)
23
(65.72%)
7.55
3
(8.56%)
7
(20.01%)
4
(11.44%)
7
(20.01%)
1
(2.85%)
1
(2.85%)
9
(25.72%)
26
(74.28%)
Discussion
According to epidemiological data from other studies,
in the general population the prevalence of CD
approaches 1% and almost 50% of the patients with
newly diagnosed CD do not present with gastrointestinal
symptoms making the diagnosis difficult [Fasamo et al.,
2003; Maki et al., 2003; Pastone et al., 2008b]. Thus,
identification of «atypical» or «silent» CD patients is
crucial. Research has shown that although the proximal
part of the intestinal mucosa represents the main site of
the intestine involved in CD, the gluten driven T-cell
activation is not restricted to the small intestine but it is
also present in the whole gastrointestinal tract [Schuppan,
2000]. The mouth as the first part of the gastrointestinal
tract, represents a very important site and the lesions of
the hard and soft tissues are of fundamental importance
as a useful diagnostic approach for the diagnosis of CD
[Aine, 1996; Poon and Nixon, 2001; Priovolou et al., 2004;
Farmakis et al., 2005; Bucci et al., 2007; Bossù et al.,
2007; de Lima et al., 2008; Pastone et al., 2008a; 2008b].
Therefore, the aim of the present study was to investigate
the periodontal condition and periodontal treatment
needs of children and teenagers with CD in Greece.
In the literature, there is also information that patients,
especially children with CD frequently complained of dry
mouth symptoms [Seyhan et al., 2007; Pastone et al.,
2008a]. This subjective sensation of dry mouth is found
together with low salivary flow and xerostomia, a
condition that could have an effect on the type of oral
microbial plaque, especially an increase of the periodontal
pathogens bacteria which could have a significant effect
on the periodontal tissues. In our study none of the
participants complained of dry mouth and our clinical
findings did not indicate any evidence of dry mouth;
therefore, we did not address the question of measuring
salivary flow and the possible role of dry mouth since our
patients did not complain of dry mouth or had any clinical
signs of dry mouth. In the present study, we have included
children over 4 years old, since at that age the deciduous
dentition is complete and the gingival tissues have
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TABLE 5 - Personal oral
hygiene conditions of 35
children and adolescents
(frequency of tooth brushing,
bleeding on brushing and
malodor).
p<0.05
p>0.05
4.60
p>0.05
completely evolved and especially the keratinised zone of
the gingival tissue is fully developed, thus giving us the
ability to thoroughly examine the oral tissues.
In the present study, two out of the 35 subjects
reported oral manifestation before the diagnosis of CD;
however, after the diagnosis of CD all subjects were
placed on a gluten-free diet and this could be the reason
for the disappearance of previous symptoms or that new
oral symptoms did not appear. The findings of the present
study are in accordance to previous studies. Bussi et al.
[2007] reported that more than one third of patients with
CD, suffering from recurrent aphthous stomatitis before
the diagnosis of CD, benefited from a gluten-free diet,
Meini et al. [1993] observed marked improvement of oral
ulcers in CD patients after one year on gluten free diet,
Majorana et al. [1992] reported that recurrent aphthous
stomatitis and intestinal histological alterations relapsed
after gluten challenge, while Campisi et al. [2008]
observed that the recurrent aphthous-like ulcers should be
considered as a risk indicator for coeliac disease but the
gluten-free diet leads to ulcer amelioration.
Additionally, the present study investigated the impact
of the co-existence of a second medical condition like
autoimmune thyroid disease and diabetes mellitus, since
these two conditions are most commonly found along
with CD. Nine subjects out of the thirty five had a second
medical condition, the presence of which had a statistically
significant correlation with the pathological oral findings.
Consequently, we could hypothesise that the second
medical condition could play an important factor in the
described changes of the periodontal tissues but also in
the need for periodontal treatment. Especially, periodontal
disease is considered to be the 6th complication of
diabetes and the application of the recent epidemiologic
methods in large populations have clearly established that
diabetes is a risk factor for periodontal disease [Mealy,
2008]. Periodontal disease in diabetic patients follows no
consistent or distinct pattern. However, a variety of
changes have been described: a tendency toward
enlarged gingiva, sessile or pedunculated gingival polyps,
polypoid gingival proliferations, abscess formation,
125
TSAMI A. ET AL.
periodontal pocketing, severe gingival inflammation, rapid
bone loss, loosened teeth. Children with type I diabetes
tend to have more destruction around the first molars and
incisors than elsewhere but this destruction becomes more
generalised at older ages
The subjects of the present study have described
bleeding when brushing, a clinical finding that describes
the presence of inflammation of the gingiva which means
presence of gingivitis. The treatment needs of the subjects
in the present study depended on the status of the oral
hygiene. In a recent study of Oulis et al. (2009) within the
population under investigation there were groups of 12
and 15 years old school children. When we compare their
findings to our findings we have noticed the following. In
the 12 years old children group the healthy periodontium
was 15.4%, in the 15 years old children group the healthy
periodontium was 16.7% whereas in our study it was
34.29%. The percentage of children with bleeding upon
probing but without need for scaling was in our study
28.57% whereas in the 12 years old children group was
41.5% and in the 15 years old children group was 30.1%.
The percentage of children with gingivitis and the need for
scaling in our study was 31.44% whereas in the 12 years
old children group was 42.7% and in the 15 years old
children group was 53.1%. Our study group seems to be
healthier than the other two groups. However, we have to
point out that these differences could be due to the
different indices that were used; in our study we used the
PSR whereas in the other study the CPITN was used, and
to the differences in determining scores 1 and 2 of these
two indices. The present study obviously has some
limitations such as the small number of patients available
for examination and the fact that all participants were
under diet. Even though, the comparable findings of the
present study with those of a previous study in a general
pediatric population could indicate that, at least in
children following a gluten-free diet, CD has not a
negative impact on the oral hygiene and the periodontal
treatment needs. The need for further longitudinal studies
on this field
in children with CD before and after
remission of the disease after a gluten-free diet is obvious.
Conclusion
The periodontal treatment needs of children and
adolescents with CD is correlated with factors that relate
to the presence of a second medical condition and to the
personal oral hygiene habits. Additionally, the oral hygiene
level and periodontal status of children with CD do not
have any specific characteristics but they have similarities
to the oral hygiene level and periodontal status of the
children of the general population.
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