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Journal of Intellectual Disability Research doi: 10.1111/jir.12629

1

Periodontal status of individuals with Down syndrome:

sociodemographic, behavioural and family
perception influence
M. A. A. Nuernberg,1 C. A. Ivanaga,1 A. N. Haas,2 A. M. Aranega,1 R. C. V. Casarin,3
R. M. S. Caminaga, V. G. Garcia5 & L. H. Theodoro1
4

1 Department of Surgery and Integrated Clinic, Division of Periodontology, School of Dentistry, São Paulo State University (UNESP),
Araçatuba, Brazil
2 Department of Periodontology, Faculty of Dentistry, Federal University of Rio Grande do Sul (UFRGS), Porto Alegre, Brazil
3 Department of Prosthodontics and Periodontics, Piracicaba Dental School, State University of Campinas (UNICAMP), Piracicaba,
Brazil
4 Department of Morphology, Araraquara Dental School, São Paulo State University (UNESP), Araraquara, Brazil
5 Post Graduate Program, Latin American Institute of Dental Research and Education (ILAPEO), Curitiba, Brazil

Abstract gingivitis and 46 (71.9%) with periodontitis. In the

multiple logistic regression final model, age and
Background The aim of the present study was to
self-reported oral hygiene practices were associated
assess the periodontal condition of individuals with
with the occurrence of periodontitis. The chance of
Down syndrome and the association with
having periodontitis was 4.7 times higher among
sociodemographic and behavioural characteristics
individuals older than 20 years and approximately 4
and family perception of oral health.
times higher in patients whose oral hygiene was per-
Methods This cross-sectional observational study
formed by themselves and their parents, compared
was performed at a referral centre for dental
with those who performed oral hygiene alone. Sex,
assistance to disabled persons in Araçatuba, Brazil.
follow-up time in the centre, education, degree of
Parents of the individuals were interviewed, and the
participants’ dependence, flossing and family history
visible plaque index, bleeding on probing, probing
of periodontal disease were not associated with the
pocket depth and clinical attachment level were
occurrence of periodontitis. Higher levels of plaque
recorded by one periodontist in six sites per tooth of
and bleeding were observed for participants with
all teeth. The individual was the unit of analysis. The
parents reporting bad gingival health (76.2% and
significance level was set at 5%.
46.9%) and deficient oral hygiene (79.5% and
Results Sixty-four subjects (23.8 ± 8.3 years old)
47.3%). The perception of parents regarding gingival
were included. Eighteen (28.1%) were diagnosed with
bleeding was correlated with higher bleeding detected
clinically (P = 0.01; 50.1%).
Correspondence: Professor Leticia Helena Theodoro, Department Conclusions The prevalence of periodontitis in
of Surgery and Integrated Clinic, Division of Periodontology, School
individuals with Down syndrome is high and
of Dentistry, São Paulo State University (UNESP), Rua José
Bonifácio, 1193, 16015-050 Araçatuba, São Paulo, Brazil (e-mail: increases with age, even in the face of the parents’
leticia.theodoro@unesp.br). perception about their children’s oral condition.

© 2019 MENCAP and International Association of the Scientific Study of Intellectual and Developmental Disabilities and
John Wiley & Sons Ltd
 Journal of Intellectual Disability Research
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M. A. A. Nuernberg et al. • Oral infections in individuals with Down syndrome
Keywords Down syndrome, health promotion,
periodontal diseases
Introduction
Down syndrome is an autosomal chromosomal
anomaly that presents high genetic complexity and
phenotype variability (Prandini et al. 2007;
Megarbane et al. 2009; Asim et al. 2015). The main
cause is the presence of an extra copy of chromosome
21 resulting in trisomy (95%), followed by
Robertsonian translocation (2–4%) and
isochromosomal or ring chromosome mosaicism
(1–2%) (Asim et al. 2015). The syndrome
represents the most common chromosomal
abnormality associated with mental deficiency
(Abanto et al. 2011) and is characterised by changes in
physical, behavioural and cognitive development.
Many abnormalities occur as part of the Down
syndrome phenotype, including motor and
musculoskeletal disorders, neurological alterations,
haematological and immunological abnormalities,
congenital heart diseases and respiratory problems
(Abanto et al. 2011).
Regarding oral manifestations, people with Down
syndrome are particularly affected by functional
problems (Hennequin et al. 2000) and an abnormal
susceptibility to infections (Levin 1987; Morgan
2007). Some studies have reported a high frequency
of gingivitis and periodontitis (Ulseth et al. 1991;
Hennequin et al. 2000; Lopez-Perez et al. 2002;
Sakellari et al. 2005; Yoshihara et al. 2005; Morinushi
et al. 2006; Cheng et al. 2007; Oredugba 2007;
Khocht et al. 2010; Al Habashneh et al. 2012;
Al-Sufyani et al. 2014). Prevalence estimates of
periodontitis in individuals with Down syndrome
under 35 years of age range between 58% and 96%
(Morgan 2007). It has been indicated that in
individuals with Down syndrome, periodontitis has
an earlier onset and presents a more severe and
generalised progression than in people without
systemic involvement (Lopez-Perez et al. 2002;
Sakellari et al. 2005).
Periodontal disease is the result of complex
interactions between the biofilm and the host’s
inflammatory immune response (Roberts & Darveau
2015), and in individuals with Down syndrome,
periodontitis is classified as a manifestation of
© 2019 MENCAP and International Association of the Scientific Study of Intellectual and Developmental Disabilities and
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systemic disease associated with genetic disorders
(Albandar et al. 2018; Jepsen et al. 2018). The
increased susceptibility to periodontal disease
observed in subjects with Down syndrome is due to
several factors, including early microbial colonisation
and composition of the microbiota (Morinushi et al.
1997; Cichon et al. 1998; Amano et al. 2000;
Ximenez-Fyvie et al. 2000; Amano et al. 2001; Khocht
et al. 2012b; Martinez-Martinez et al. 2013), impaired
immune response and increased gingival
inflammation (Barr-Agholme et al. 1998; Otsuka et al.
2002; Tsilingaridis et al. 2003; Iwamoto et al. 2009;
Yamazaki-Kubota et al. 2010; Tanaka et al. 2012;
Khocht et al. 2012a; Khocht et al. 2014).
Additionally, the family structure may have a
significant role in the prevalence of periodontitis
(Kaye et al. 2005; Zizzi et al. 2014; Descamps & Marks
2015), and the periodontal profile of this population
may also be associated with the intelligence quotient
of the patient and the educational level of the parents
(Al-Sufyani et al. 2014). The participation of the
parents in supervising/performing oral hygiene is
essential for prevention and control of periodontal
disease in this population (Ferreira et al. 2016).
However, very few attempts within the medical
scientific literature have been made to describe and
understand parents’ perception of periodontal disease
and its contribution to maintaining the oral hygiene of
their children (Kaye et al. 2005; Al-Sufyani et al. 2014;
Zizzi et al. 2014; Descamps & Marks 2015).
In order to extend the knowledge of the periodontal
status of individuals with Down syndrome within the
family context, the present study assessed the
periodontal condition and evaluated the effect of
sociodemographic, behavioural and family perception
factors on the periodontal profile of individuals with
Down syndrome under dental outpatient follow-up at
a referral centre.
Methods
Study design and sample selection
The present cross-sectional observational study was
carried out between September 2017 and March
2018, following the norms of the STROBE statement
(von Elm et al. 2008), and was approved by the local
Human Research Ethics Committee (CAAE no.
76483917.8.0000.5420). The research was developed
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M. A. A. Nuernberg et al. • Oral infections in individuals with Down syndrome
at the Dental Assistance Center for Disabled Persons
(CAOE) of the São Paulo State University (UNESP),
School of Dentistry, Araçatuba, Brazil.
All patients diagnosed with Down syndrome
under dental outpatient follow-up at the
CAOE centre, during the period of the study,
were invited to participate in the periodontal
evaluation before receiving dental care by
professionals from the auxiliary unit. Those
responsible for the participants were individually
informed about the nature of the study and gave
written informed consent.
The inclusion criteria were patients previously
diagnosed with Down syndrome older than 13 years
of age. Subjects unable to cooperate during the
periodontal examination (mainly due to intellectual
disability), patients with unstable health conditions,
patients with haematological diseases or active cancer
and patients requiring sedation or general anaesthesia
were excluded from the study.
Sample size
The sample size was calculated from a finite
population of 187 patients with Down syndrome
under dental outpatient follow-up at CAOE. A
prevalence of 90% was considered for the occurrence
of periodontitis in people with Down syndrome,
reported in the scientific literature (Morgan 2007;
Khocht & Albandar 2014) and a required accuracy of
5% (0.05). The minimum sample required for a 90%
confidence interval was 64 subjects (Lwanga 1991).
The sample size calculation was performed using Epi
Info™ software 7.2.1.0 (Centers for Disease Control
and Prevention, Atlanta, USA).
Sociodemographic and behavioural factors and
family perception
A structured questionnaire was filled out by direct
interview with the parents of the participants, prior to
the clinical examination. The questionnaire was
applied by one researcher (C. A. I.) and was divided
into four sections:
1 Personal information: age, gender, time of care at
the CAOE centre and parents’ level of education.
2 Systemic and Down syndrome characteristics:
systemic conditions, type of diet, use of medica-
tions, degree of dependence for daily activities
© 2019 MENCAP and International Association of the Scientific Study of Intellectual and Developmental Disabilities and
John Wiley & Sons Ltd
and degree of dependence for oral hygiene
(Zizzi et al. 2014).
3 Dental evaluation: oral hygiene habits of their
children with questions related to the frequency
of daily brushing, use of mouthwash and
toothbrush, brush type and family history of
periodontal disease.
4 Family perception: knowledge and family percep-
tion about the oral health of their children. The
questions were adapted from a questionnaire re-
lated to the quality of life of individuals with
Down syndrome (Amaral Loureiro et al. 2007)
and from a qualitative study about views and
knowledge, regarding dental care, of parents
who have a child with Down syndrome
(Descamps & Marks 2015). Parents were
questioned about their perception of gum health
and oral hygiene and perception about any
problem/discomfort in the mouth and gingival
bleeding.
Clinical periodontal parameters
The following clinical parameters were evaluated:
visible plaque index (presence or absence), bleeding
on probing (BOP), probing pocket depth (PPD),
clinical attachment level (CAL) and number of lost
teeth. BOP was determined in terms of the presence
(+) or absence ( ) of bleeding during the 30 s after
the first probe insertion in the pocket (Armitage 2004;
Holtfreter et al. 2015). All these clinical parameters
were performed by a calibrated examiner
(M. A. A. N.) with a periodontal probe (PCPUNC-
15, Hu-Friedy, Chicago, IL, USA) in all present teeth
at six sites per tooth (mesiobuccal, midbuccal,
distobuccal, distolingual, midlingual and
mesiolingual), excluding third molars.
The diagnosis of periodontitis was determined
according to the criteria proposed by the periodontal
disease classification system of the Armitage (1999).
Calibration of examiners
The proposed indicators were recorded at six sites of
index teeth (17–16, 11, 26–27, 36–37, 31 and 46–47) of
10 individuals at two different moments (7-day
interval). The analysis of intra-rater agreement of
PPD and CAL variables was obtained through the
 Journal of Intellectual Disability Research
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M. A. A. Nuernberg et al. • Oral infections in individuals with Down syndrome
intraclass correlation coefficient, and the calibration
was considered satisfactory (0.92).
Statistical analysis
Comparisons of variables with normal distribution
were conducted with the t-test and analysis of
variance, whereas for non-normal data, the
comparisons were made by the Mann–Whitney
U-test. Data are described by the frequency
distribution and means with standard deviations.
Simple and multiple logistic regression models
were fitted for the primary outcome of this study
(periodontitis). Independent variables included in the
analyses were between sociodemographic (age,
gender and parents’ education level), behavioural
(degree of dependence, oral hygiene, dental floss,
antiseptic and family history of periodontal disease)
and family perception factors and diagnosis of
periodontal disease. Variables with P values <0.25 in
the simple models were entered in an initial multiple
model. The maintenance of the variables in the final
model was determined by P values <0.05 and the
presence of confounding effects.
The statistical analysis was conducted with a
specific analytical package (STATA for Macintosh,
version 14, Stata Corp, TX, USA). The individual
was the unit of analysis. The significance level was set
at 5%.
Results
During the period of data collection, a total of 187
individuals who were being attended at the CAOE
centre were eligible for the study. Eighty-two
individuals with Down syndrome and their parents
agreed to participate in the study. Of these, 14 were
not able to receive dental clinical evaluation due to
cognitive or systemic impairment. Sixty-eight subjects
were considered eligible according to the inclusion
and exclusion criteria; however, two participants were
subsequently excluded because of sensitivity and
impatience during the clinical examination and two
participants because of lack of data.
A total of 64 individuals (24 females and 40 males)
between 14 and 51 years (mean age 23.8 ± 8.3 years)
were included in the study. Overall, the individuals
presented high levels of plaque (66.58%). The median
for bleeding reached 30.6% of sites. The median
© 2019 MENCAP and International Association of the Scientific Study of Intellectual and Developmental Disabilities and
John Wiley & Sons Ltd
percentages of sites with PPD and CAL ≥4 mm were
3.1% and 5.9%, respectively (Fig. 1). Mean PPD and
CAL were 2.4 ± 0.5 mm and 2.6 ± 0.7 mm,
respectively. Forty-five (70.3%) subjects had one or
more site with PPD ≥4 mm, 28 (43.75%) of them had
at least one site with PPD 5–6 and 8 (12.5%)
individuals had at least one PPD ≥7 mm. With regard
to the periodontal diagnosis, 18 (28.1%) had gingivitis
and 46 (71.9%) had localised (62.5%) or generalised
(9.4%) periodontitis.
Periodontitis was significantly more prevalent in
individuals older than 20 years of age (Table 1). In the
multiple final model, age and self-reported oral
hygiene practices were associated with the occurrence
of periodontitis. Individuals older than 20 years had a
4.7 times higher chance of presenting periodontitis
than those between 14 and 20 years. The chance of
having periodontitis was approximately 4 times higher
in patients whose oral hygiene was performed by
themselves and their parents, compared with those
who perform oral hygiene alone (Table 2).
None of the evaluated predictors were related to the
levels of plaque (Table 3), except the self-reported use
of antiseptics, which was associated with lower levels
of plaque (55.5% compared with 75.2%). Older
patients presented a higher percentage of bleeding
(43.2%) than younger patients (30.7%). A lower
number of lost teeth were observed for patients with a
partial degree of dependence and for those dependent
for oral hygiene practices.
Figure 1 Boxplot for the percentage of sites with visible plaque
index (VPI), bleeding on probing (BOP), probing pocket depth
(PPD) and clinical attachment level (CAL) ≥4 mm for the whole
sample. [Colour figure can be viewed at wileyonlinelibrary.com]
 Journal of Intellectual Disability Research
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M. A. A. Nuernberg et al. • Oral infections in individuals with Down syndrome

Table 1 Distribution of individuals with gingivitis and periodontitis with higher bleeding detected clinically (50.1%).
according to predictors
None of the variables related to parents’ knowledge
were associated with tooth loss.
Whole
sample (n) Gingivitis Periodontitis P
Discussion
Age (years) The present study evaluated the periodontal
14–20 27 12 (44.4) 15 (55.6)
condition of individuals with Down syndrome who
>20 37 6 (16.2) 31 (83.8) 0.02
Gender were under dental outpatient follow-up and assessed
Female 24 9 (37.5) 15 (62.5) the effect of sociodemographic factors, behavioural
Male 40 9 (22.5) 31 (77.5) 0.25 characteristics and the parents’ perception regarding
Time of care (years) their children’s periodontal health. The occurrence of
≤3 18 4 (22.2) 14 (77.8)
periodontitis in the studied population was found to
>3 46 14 (30.4) 32 (69.6) 0.76
Parents’ educational level be associated with age and oral hygiene habits.
<Incomplete 33 9 (27.3) 24 (72.7) Despite the parents’ ability to perceive poor oral
high school hygiene and some changes related to their children’s
>High school 31 9 (29.0) 22 (71.0) 1.00 periodontal disease, an inefficient plaque control, a
Degree
considerable bleeding percentage and a high
of dependence
Independent 24 8 (33.3) 16 (66.7) prevalence of periodontitis were the main findings.
Partially 40 10 (25.0) 30 (75.0) 0.57 Similar to previous studies with individuals with
dependent Down syndrome (Yoshihara et al. 2005; Zizzi et al.
Dependence for 2014), age was highlighted as an important factor in
oral hygiene
the occurrence of periodontitis. This relationship is
Self-sufficient 36 10 (27.8) 26 (72.2)
Dependent 28 8 (28.6) 20 (71.4) 1.00 also found in the general population. Besides age,
Oral hygiene some epidemiological studies have shown that
Alone 24 10 (41.7) 14 (58.3) periodontal disease is also related to a series of socio-
Parents 17 4 (23.5) 13 (76.5) economic factors such as low educational level and
Both 23 4 (17.4) 19 (82.6) 0.16
social class, as well as with male gender, black or
Dental floss
Yes 24 7 (29.2) 17 (70.8) mixed colour and smoking (Bonfim et al. 2013;
No 40 11 (27.5) 29 (72.5) 1.00 Almerich-Silla et al. 2017). Our results demonstrated
Antiseptic that individuals older than 20 years had a 4.7 times
Yes 28 7 (25.0) 21 (75.0) higher chance of developing periodontitis than those
No 36 11 (30.6) 25 (69.4) 0.78
between 14 and 20 years. However, different from
Family history of PD
Yes 35 6 (24.0) 19 (76.0) previous evidence (Al-Sufyani et al. 2014), parental
No 39 12 (30.8) 27 (69.2) 0.78 educational level was not associated with plaque,
Total 64 18 (28.1) 46 (71.9) BOP, tooth loss, gingivitis or periodontitis.
The periodontal condition found in the individuals
PD, periodontal disease. of the present study was quite similar to the findings
from the literature. In a previous study, 85% of
The occurrence of periodontitis was significantly subjects with Down syndrome (aged 17–42 years)
higher when the parents evaluated the gingival and presented at least one site with PPD ≥4 mm, and 49%
dental health of their children as bad and when of them had at least one site with PPD ≥6 mm (Cheng
parents believed their children may experience et al. 2007). In the present study, 70.3% subjects had
discomfort because of their oral health status one or more site with PPD ≥4 mm, 43.8% of them
(Table 4). Higher levels of plaque and bleeding were had at least one site with PPD 5–6 and 12.5% of
observed for patients whose parents reported bad individuals had at least one PPD ≥7 mm. Regarding
gingival health (76.2% and 46.9%) and deficient oral mean PPD, this study found 2.4 ± 0.5 mm, similar to
hygiene (79.5% and 47.3%). The perception of a study with Jordanian children with Down syndrome
parents regarding gingival bleeding was correlated (12–16 years) attending special needs centres

© 2019 MENCAP and International Association of the Scientific Study of Intellectual and Developmental Disabilities and
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 Journal of Intellectual Disability Research
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M. A. A. Nuernberg et al. • Oral infections in individuals with Down syndrome

Table 2 Simple and multiple logistic regression models for predictors of periodontitis

Simple models Multiple final model

OR (95% CI) P OR (95% CI) P

Age (years)
14–20 1 1
>20 4.13 (1.30–13.15) 0.02 4.69 (1.38–15.09) 0.01
Gender
Female 1
Male 2.07 (0.68–6.27) 0.20
Time of care (years)
≤3 1
>3 0.65 (0.18–2.34) 0.51
Parents’ educational level
<Incomplete high school 1
>High school 0.92 (0.30–2.73) 0.88
Degree of dependence
Independent 1
Partially dependent 1.50 (0.49–4.55) 0.47
Dependence for oral hygiene
Self-sufficient 1
Dependent 0.96 (0.32–2.89) 0.94
Oral hygiene
Alone 1 1
Parents 2.32 (0.58–9.26) 0.23 2.58 (0.59–11.33) 0.21
Both 3.39 (0.89–13.10) 0.08 4.07 (1.01–17.26) 0.04
Dental floss
Yes 1
No 1.09 (0.35–3.33) 0.89
Antiseptic
Yes 1
No 0.76 (0.25–2.30) 0.62
Family history of PD
Yes 1
No 0.71 (0.22–2.23) 0.56

CI, confidence interval; OR, odds ratio; PD, periodontal disease.

(2.3 ± 0.2 mm) (Al Habashneh et al. 2012). Higher
PPD means were found in Japanese children aged
6–18 (2.89 ± 0.43) (Yamazaki-Kubota et al. 2010)
and in patients who attended in a centre for the
disabled in Jerusalem with a mean age of
23.3 ± 4 years (3.1 ± 0.94) (Zigmond et al. 2006).
The mean CAL (2.6 ± 0.7 mm) was slightly higher
than the mean PPD (2.4 ± 0.5 mm) in this study; this
clinical finding contributes to the presumption that,
in subjects with Down syndrome, periodontal
destruction increases with age and increasingly
appears as total attachment loss rather than increased
pocket depth (Sakellari et al. 2005).
The majority of the parents reported helping their
children to carry out oral hygiene (62.5%), reinforcing
the patient’s previous hygiene (35.9%) or performing
tooth brushing completely (26.5%). These
proportions are similar to those reported in previous
studies, in which the percentages of parents who
helped their child during tooth brushing on a daily
basis were 60% (Hennequin et al. 2000) and 58%
(Descamps & Marks 2015). Paradoxically, our results
showed that the chance of presenting periodontitis
was approximately 4 times higher in patients whose
oral hygiene was performed by themselves and their
parents, compared with those who performed oral

© 2019 MENCAP and International Association of the Scientific Study of Intellectual and Developmental Disabilities and
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M. A. A. Nuernberg et al. • Oral infections in individuals with Down syndrome

Table 3 Percentages of sites with plaque and bleeding and number of lost teeth (mean ± standard deviation) according to predictors

VPI P BOP P Tooth loss P

Age (years)
14–20 63.1 ± 30.3 30.7 ± 21.9 2.3 ± 2.5
>20 69.1 ± 28.6 0.42 43.2 ± 25.7 0.04 3.5 ± 5.2 0.83
Gender
Female 58.9 ± 33.3 38.5 ± 26.9 3.6 ± 5.4
Male 71.2 ± 25.9 0.10 37.5 ± 23.8 0.89 2.6 ± 3.4 0.81
Time of care (years)
≤3 65.9 ± 36.3 40.4 ± 26.7 4.5 ± 6.1
>3 66.9 ± 26.5 0.91 36.9 ± 24.3 0.62 2.4 ± 3.2 0.32
Parents’ educational level
<Incomplete high school 67.9 ± 30.4 39.5 ± 27.1 3.4 ± 4.9
>High school 65.2 ± 28.4 0.71 36.1 ± 22.5 0.58 2.5 ± 3.6 0.55
Degree of dependence
Independent 66.5 ± 27.1 36.3 ± 27.4 5.0 ± 5.9
Partially dependent 66.6 ± 30.8 0.99 38.8 ± 23.4 0.69 1.8 ± 2.2 0.01
Dependence for oral hygiene
Self-sufficient 66.1 ± 28.7 34.3 ± 23.8 3.6 ± 4.5
Dependent 67.2 ± 30.5 0.88 42.5 ± 25.8 0.19 2.2 ± 3.8 0.04
Oral hygiene
Alone 63.2 ± 30.9 34.6 ± 27.5 4.0 ± 5.3
Parents 75.3 ± 28.5 44.7 ± 24.4 2.6 ± 4.8
Both 63.6 ± 27.9 0.36 36.2 ± 22.2 0.41 2.2 ± 2.0 0.20
Dental floss
Yes 67.9 ± 29.4 31.8 ± 21.4 2.3 ± 2.3
No 65.8 ± 29.5 0.77 41.5 ± 26.3 0.13 3.4 ± 5.1 0.94
Antiseptic
Yes 55.5 ± 29.7 38.6 ± 25.8 3.4 ± 5.1
No 75.2 ± 26.2 0.01 37.3 ± 24.4 0.84 2.7 ± 3.6 0.71
Family history of PD
Yes 69.7 ± 28.6 36.4 ± 20.1 2.6 ± 4.2
No 64.6 ± 29.8 0.49 38.8 ± 27.7 0.71 3.2 ± 4.3 0.15

BOP, bleeding on probing; PD, periodontal disease; VPI, visible plaque index.

hygiene alone. This may possibly be explained by the
greater involvement of parents in the control of
hygiene when they notice gingival
inflammation/bleeding or signs of periodontal
destruction.
Individuals categorised by their parents as
independent for daily activities had more tooth loss
than partially dependent individuals. Those
considered self-sufficient for oral hygiene practices
also presented a higher number of lost teeth. These
results may be due to an overestimated perception of
parents as to their children’s ability to perform
brushing without supervision.
The present results also showed that the use of
antiseptics was associated with lower plaque levels.
Faced with the inability of people with Down
syndrome to effectively control supragingival
plaque, even with parental assistance,
recommending the use of antiseptics may be a
useful prevention tool. Individuals with Down
syndrome experience very early colonisation by
various periodontal pathogens in their childhood
(Cichon et al. 1998; Amano et al. 2001; Sakellari
et al. 2005). Recent studies have suggested that
supragingival plaque may affect the subgingival
plaque composition, acting as a reservoir of
periodontal pathogens for the dissemination or
reinfection of subgingival sites (Ximenez-Fyvie et al.
2000) and, consequently, affecting clinical indices of
periodontal patients with Down syndrome (Sakellari
et al. 2005). Chemical adjuvants seem to improve
periodontal outcomes in the preventive and

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 Journal of Intellectual Disability Research
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M. A. A. Nuernberg et al. • Oral infections in individuals with Down syndrome

Table 4 Knowledge regarding oral health reported by parents and oral health status

Periodontitis VPI BOP Tooth loss

n (%) P (mean ± SD) P (mean ± SD) P (mean ± SD) P

Think that their child may have gingival disease

Yes 9 (81.8) 68.6 ± 25.2 44.8 ± 25.9 4.4 ± 5.2
No 37 (69.8) 0.71 66.1 ± 30.2 0.80 36.4 ± 24.6 0.31 2.7 ± 4.1 0.15
Evaluation of child’s gingival and dental health
Good 21 (60.0) 58.6 ± 28.5 30.3 ± 20.9 2.6 ± 3.3
Bad 25 (86.2) 0.03 76.2 ± 27.7 0.02 46.9 ± 26.5 0.01 3.5 ± 5.3 0.86
Evaluation of oral hygiene of their child
Satisfactory 24 (63.9) 57.2 ± 28.9 31.0 ± 19.5 2.6 ± 3.5
Deficient 22 (81.5) 0.17 79.5 ± 24.9 0.002 47.3 ± 28.4 0.01 3.6 ± 5.2 0.62
Believe that the oral health status of their child may cause discomfort
Yes 11 (52.4) 67.4 ± 29.5 42.3 ± 28.9 3.5 ± 5.2
No 35 (81.4) 0.02 66.2 ± 29.5 0.88 35.7 ± 22.6 0.32 2.7 ± 3.8 0.73
The gingiva of the child usually bled
Yes 18 (90.0) 75.7 ± 26.1 50.1 ± 24.9 3.0 ± 4.8
No 28 (63.6) 0.04 62.4 ± 29.9 0.10 32.3 ± 23.0 0.01 2.9 ± 4.1 0.74

BOP, bleeding on probing; SD, standard deviation; VPI, visible plaque index.

periodontal treatment of patients with Down
syndrome (Ferreira et al. 2016).
Regarding the evaluation of the parents’
perception, the present study made an important
contribution to understanding the family context of
these individuals and the vision of periodontal health
from the perspective of the parents. A qualitative
study, which investigated parents’ experiences and
expectations, suggested that attitudes and skills of
dental health professionals, behavioural problems,
feelings of stigma, the relatives’ expectations about
dentists, their oral health beliefs, information and
support received, as well as their knowledge and
priorities, may influence experiences in oral health
care (Kaye et al. 2005). Results from our study
showed that many parents were able to notice
deficient hygiene and gingival bleeding in their
children. Moreover, in the presence of periodontitis,
many of them noticed the change in the oral condition
and evaluated their children’s oral and dental health
as ‘bad’ and said that they believed that their children
might experience some discomfort due to their oral
health condition.
In summary, parents were able to observe some
periodontal changes, and many of them reported
helping their children to perform tooth brushing, but
these factors are not enough to maintain their
children’s periodontal health. This scenario leads us
to reflect on the difficulty that most parents have to
achieve good plaque control and the need to reinforce
guidelines and hygiene techniques at each visit. It also
indicates the importance of periodic professional
intervention for this group of patients.
Even though the patients of this study were enrolled
in a specialised dental follow-up programme, more
than half of them had periodontitis, and the follow-up
time in the service was not statistically related to any
of the clinical outcomes studied. Although
unsatisfactory, this result corroborates some previous
studies that demonstrated a limited effect of dental
care programmes in the control of progression of
periodontitis in patients with Down syndrome
(Cichon et al. 1998; Zigmond et al. 2006; Khocht et al.
2010). A 7-year longitudinal study, which evaluated
radiographic bone loss, also demonstrated that
periodic dental appointments were not effective in
controlling the progression of periodontal disease in
these patients (Agholme et al. 1999). Controversially,
studies that presented continuous, systematic and
individualised preventive dental care with close
monitoring and frequent professional supragingival
cleaning and prophylaxis demonstrated an effective
improvement in periodontal health in this special
group of patients (Sakellari et al. 2001; Yoshihara et al.
2005; Cheng et al. 2007). In a global view,
establishing efficient protocols or adjuvant

© 2019 MENCAP and International Association of the Scientific Study of Intellectual and Developmental Disabilities and
John Wiley & Sons Ltd
 Journal of Intellectual Disability Research
9
M. A. A. Nuernberg et al. • Oral infections in individuals with Down syndrome
periodontal strategies to reduce the probability of
reinfection and disease progression, with consequent
improvement in dental maintenance, is still a
challenge, independently of the population studied
(Manresa et al. 2018).
Therefore, the present study indicates that the
inclusion of these patients in a prevention programme
and the perception of parents on the poor oral health
in these individuals may not be enough to reduce the
occurrence of periodontal disease in this group of
patients. This result emphasises the hypothesis that
for subjects with Down syndrome, periodontal
disease could be associated with factors other than, or
in addition to, oral hygiene (Zizzi et al. 2014).
The compromised immunity of patients with Down
syndrome, added to an altered inflammatory response
in the presence of plaque, makes these individuals
more susceptible to the development of periodontal
disease (Albandar et al. 2018; Scalioni et al. 2018).
Studies have shown that subjects with Down
syndrome present reduced activity of neutrophils and
T lymphocytes, as well as increased production of
inflammatory mediators and proteolytic enzymes,
such as prostaglandin E2, leukotriene B4 and matrix
metalloproteinases (Tsilingaridis et al. 2003;
Morgan 2007). Other factors that may explain the
periodontal status of patients with Down syndrome
include functional problems (e.g. open-mouth
breathing, tooth morphology, macroglossia and
malocclusion), early colonisation by various
periodontopathogens and higher levels of some
subgingival bacterial species (Amano et al. 2001;
Morgan 2007; Khocht et al. 2012b).
The present data also suggest that the current
strategy for prevention and periodontal treatment in
the centre studied may not be enough or that the
frequency of dental appointments needs adjustment,
considering the obvious challenge found in patients
with Down syndrome. Although the period between
dental appointments was not the object of this study,
the referred assistance centre is a regional reference
for the dental care of disabled persons, receiving
patients from different cities. The majority of the
patients attending this centre have a low socio-
economic level and great difficulties to move from
their home cities to receive treatment. Thus, although
the CAOE represents the only oral care alternative for
these patients, many families do not follow regular
dental follow-up due to social limitations, such as the
© 2019 MENCAP and International Association of the Scientific Study of Intellectual and Developmental Disabilities and
John Wiley & Sons Ltd
need for public transportation services. Future studies
should consider the interval between dental
appointments to indicate a satisfactory follow-up
frequency according to the different degrees of
physical, behavioural and cognitive impairment of
individuals with Down syndrome.
The major limitation of this study was the sampling
process. Unfortunately, we could only include
individuals with Down syndrome who were able to
cooperate and sit through the study examinations
without the need for sedation or restraint. Probably, if
the non-cooperative and violent patients, who fail to
communicate well, or need to be restrained or
sedated for an examination, had been included, there
would be a greater possibility of finding worse oral
hygiene and periodontal status. Therefore, the results
may not extend to individuals with Down syndrome
with major cognitive impairment.
Despite the high prevalence of systemic
co-morbidities, after the onset of antibiotics and
the possibility of surgical treatment for congenital
heart defects, the life expectancy of patients with
the syndrome has increased significantly (Yang et al.
2002), and the maintenance of good periodontal
health is fundamental to guarantee the quality of life
of these patients (Amaral Loureiro et al. 2007). The
information obtained in this study will not only aid
our understanding of the sociodemographic,
behavioural and family perception influence on
periodontal disease but will also guide the
development of appropriate preventive and
treatment strategies for patients with Down
syndrome. The family environment plays a
fundamental role in the stimulus for the hygiene care
of patients with Down syndrome (Zizzi et al. 2014).
However, this study demonstrated that plaque
control and periodontal prevention go beyond the
awareness and guidance of family members. In view
of the complexity of these patients, it is essential that
periodontal prevention and treatment are not
underestimated (Scalioni et al. 2018).
Individuals with Down syndrome presented a high
prevalence of periodontitis, mainly related to age.
Despite the parents’ ability to perceive the deficient
oral condition of their children, parents showed
limited capacity to perform effective plaque control.
Therefore, the present study suggests that family care
may not be sufficient for the prevention and control of
periodontal diseases in this group with higher
 Journal of Intellectual Disability Research
10
M. A. A. Nuernberg et al. • Oral infections in individuals with Down syndrome
susceptibility. The implementation of a continuous
preventive dental care programme with very close
monitoring and frequent professional supragingival
cleaning and prophylaxis seems to be a necessary
strategy to achieve periodontal health, especially for
those individuals who are able to cooperate without
the need for sedation or restraint.
Acknowledgements
The authors thank the collaboration of all staff from
the Dental Assistance Center for Disabled Persons
(CAOE) of the São Paulo State University (UNESP),
School of Dentistry, Araçatuba, Brazil, as well as the
patients with Down syndrome and their families for
their participation in this study.
Conflict of interest
The authors report no conflicts of interest related to
this study.
Source of funding
This research did not receive any specific grant from
funding agencies in the public, commercial, or not-
for-profit sectors.
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Accepted 26 March 2019