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Journal of Intellectual Disability Research doi: 10.1111/j.1365-2788.2006.00794.

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Blackwell Science, LtdOxford, UKJIRJournal of Intellectual Disability Research-Blackwell Publishing Ltd, 7492500Original ArticleOutcome of a preventive dental programme on periodontal status in Downs syndromeZ. Maora et al.

The outcome of a preventive dental care programme on


the prevalence of localized aggressive periodontitis in
Downs syndrome individuals
M. Zigmond,1 A. Stabholz,2 J. Shapira,3 G. Bachrach,1 G. Chaushu,4 A. Becker,5 E. Yefenof,6
J. Merrick7 & S. Chaushu5
1 Hadassah School of Dental Medicine, Institute of Dental Sciences, Hebrew University, Jerusalem, Israel
2 Department of Periodontics, Hadassah School of Dental Medicine, Hebrew University, Jerusalem, Israel
3 Department of Pediatric Dentistry, Hadassah School of Dental Medicine, Hebrew University, Jerusalem, Israel
4 Department of Oral and Maxillofacial Surgery, The Tel Aviv Souraski Medical Center, Tel Aviv, Israel
5 Department of Orthodontics, Hadassah School of Dental Medicine, Hebrew University, Jerusalem, Israel
6 Lautenberg Center of General and Tumor Immunology, Hadassah School of Medicine, Hebrew University, Jerusalem, Israel
7 National Institute of Child Health and Human Development, Office of the Medical Director, Division for Mental Retardation,
Ministry of Labour and Social Affairs, Jerusalem, Israel

Abstract Results In spite of similar oral hygiene and gingival


measures, DS patients, as opposed to the control
Background Periodontal disease in Downs syn-
ones, had a severe periodontal disease. The preva-
drome (DS) individuals develops earlier and is more
lence, extent and severity of periodontitis in the DS
rapid and extensive than in age-matched normal indi-
group were significantly greater than in the control
viduals. The present study evaluated a group of DS
group. The teeth most commonly and severely
patients, who had been participating in a -year
affected were the lower central incisors and the upper
preventive dental programme, for the impact of the
first molars. DS patients lost significantly more teeth
programme on their periodontal status.
due to periodontitis.
Methods Thirty DS patients (mean age
Conclusions The clinical and radiographic picture
. years) were compared with age-matched
found in the present DS group is characteristic
healthy controls (mean age . years). The
of localized aggressive periodontitis. Within the
hygiene level, gingival condition and periodontal
limitations of this study, it seems that the preventive
status (periodontal probing depth, clinical attach-
dental programme had no effect on periodontal
ment level and radiographic alveolar bone loss) were
destruction progression of localized aggressive
determined.
periodontitis in DS individuals and that impaired
oral hygiene plays a relatively minor role in the
Correspondence: Zigmond Maora, Hadassah School of Dental
pathogenesis of this disease. Future controlled
Medicine, Institute of Dental Sciences, Hebrew University, PO Box studies are needed to assess the effectiveness
, Jerusalem Israel (e-mail: maora@md.huji.ac.il). of different preventive dental programmes in
The Authors. Journal Compilation Blackwell Publishing Ltd
Journal of Intellectual Disability Research
493
Z. Maora et al. Outcome of a preventive dental programme on periodontal status in Downs syndrome

preventing the progression of periodontitis in DS tion were carried out in Israel (Shapira et al. ;
patients. Stabholz et al. ). Based on their findings, a com-
prehensive preventive dental health programme was
Keywords aggressive periodontitis, dental
implemented in this population (Shapira & Stabholz
preventive programme, Downs syndrome
). Following months of this preventive dental
health programme, a significant improvement in the
patients plaque, gingival and bleeding indices was
Introduction
achieved. However, parameters of periodontitis
Downs syndrome (DS) is an autosomal genetic dis- severity were not evaluated in both studies due to the
order, caused by an extra chromosome , with an young age of the patients and lack of compliance.
incidence of / live births. The syndrome is char- Today, the preventive dental programme is ongoing
acterized by intellectual disability and phenotypic and includes the entire DS population of that specific
abnormalities including oral, cardiovascular, hae- institution. The aim of the present study was there-
matopoietic, musculoskeletal, nervous and behav- fore to evaluate the periodontal status of DS patients
ioural anomalies. Subjects with DS are prone to the undergoing a preventive dental health programme
development of infectious, malignant and autoim- and to compare it with that of age-matched healthy
mune diseases (Desai ). Dental characteristics controls.
have included missing teeth, delayed eruption, late
developing dentitions, impacted maxillary canines
and malocclusions such as crowding, posterior cross- Materials and methods
bite and anterior open bite (Roger ; Shapira et al.
Patients
).
Few studies have reported that DS individuals have The experimental study group included patients
an increased prevalence of periodontal disease com- with DS (mean age . years, females and
pared with otherwise normal, age-matched control males), each exhibiting typical chromosome tri-
groups and other mentally handicapped patients of somy. All the patients attended the Elwyn Center for
similar age distribution (Cutress ; Orner ; the Disabled in Jerusalem, Israel, either as full-time
Saxen et al. ; Barnett et al. ; Reuland-Bosma or as residents living in hostel-like apartments, and
& van Dijk ). The prevalence of periodontitis have been participating in a dental preventive pro-
under the age of may reach up to % and is in gramme for the last years (Shapira & Stabholz
sharp contrast with the low incidence of carious ). The programme included oral hygiene instruc-
lesions (Orner ). The progression and severity as tion given to the home carers (parents or guardians),
well as the clinical characteristics of the periodontal as well as supragingival and subgingival scaling pro-
destruction reported in DS subjects are consistent vided every months by a trained dental hygienist.
with the early-onset/aggressive periodontitis disease The compliance (in terms of attendance) of the
pattern (Shaw & Saxby ; Cichon et al. ). patients included in this study was excellent because
Aggressive periodontitis is characterized by an early their home carers brought them to the dental clinic
age of onset, rapid rate of disease progression and on a strictly scheduled basis.
severe destruction of periodontal tissues which can- The control group consisted of age-matched
not be attributed solely to poor oral hygiene. Addi- healthy volunteers (mean age . years,
tional risk factors such as immunological deficiencies females and males) that included either students or
and early senescence have been suggested to underlie employees of the Faculty of Dental Medicine in
this group of periodontal diseases (Reuland-Bosma Jerusalem. They were asked to provide a personal
& van Dijk ; Shaw & Saxby ). However, the medical history to confirm the absence of systemic
aetiology is not yet fully understood. disorders or medication known to affect the peri-
Most surveys on periodontal disease in DS have odontal condition. Only half of them (%) had
been carried out in Europe and the United States; received scaling and root planning treatment by a
two controlled studies that evaluated periodontal dental hygienist during the months prior to the
treatment needs of an institutionalized DS popula- examination.
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Journal of Intellectual Disability Research
494
Z. Maora et al. Outcome of a preventive dental programme on periodontal status in Downs syndrome

All participants provided informed consent (in the were calculated for each individual. The number of
case of DS subjects by a parent or guardian) to a teeth that had been lost due to periodontitis was
protocol that was reviewed and approved by the insti- recorded as well.
tutional ethics committee. Radiographic alveolar bone loss was assessed by
measuring the distance between CEJ and the alveolar
bone crest [which is referred to as radiographic bone
Clinical and radiographic examinations
loss (RBL)] on a set of bite-wings and anterior
Eight index teeth were examined in each patient (per- periapical radiographs (E-speed films, Kodak, Roch-
manent upper and lower central incisors and all first ester, NY, USA), taken using a standardized long
permanent molars). These teeth were chosen based cone technique. The radiographs were developed,
on previous studies which showed that they are pri- scanned and magnified six-fold by Microsoft Photo-
marily affected by periodontal disease in DS patients shop software. The measurements were performed on
(Cohen et al. ; Jhonson & Young ; Sznajder the mesial and distal aspects of each tooth examined,
et al. ; Cutress ; Modeer et al. ; with the aid of a Vernier caliper (Dentaurum,
Agholme et al. ). It was impossible to perform a Pforzheim, Germany), to the nearest . mm. A site
full-mouth periodontal examination in these patients was considered to be periodontally affected when
because of their poor compliance. The clinical exam- RBL mm (Kallestal & Matsson ).
inations were performed by one author (A.S.) and the
radiographs were taken by another (M.Z.). DS
Statistical analysis
patients with cardiac anomalies who needed infective
endocarditis (IE) prophylaxis were given g amox- Differences between the test and control groups were
icillin (Dajani et al. ) one hour before the peri- analysed using chi-squared test, Fishers exact test
odontal examination. and Wilcoxons test. The data analysis was processed
The periodontal examination was carried out using using the statistical analysis software SAS. All P-
a dental mirror and a UNC- periodontal probe. values were based on two-tailed tests, and P < .
The presence or absence of supragingival plaque was was the criterion of significance.
recorded at four surfaces per tooth (mesio-buccal,
disto-buccal, mesio-lingual and disto-lingual) and the
Error of the method
plaque score calculated (per cent of tooth surfaces
with plaque). The errors of the clinical and radiographic measure-
The presence or absence of bleeding on probing ments were assessed by analysing two sets of mea-
(BOP) was evaluated on a dichotomous scale at six surements made a week apart on control patients,
sites per tooth (mesio-buccal, mid-buccal, disto- and on radiographic views selected at random,
buccal, mesio-lingual, mid-lingual and disto-lingual) according to the method of Dahlberg (). The
and expressed as a percentage of the total number of errors were: for PPD . mm, CAL . mm and
sites examined. RBL . mm and were considered to be insignifi-
Pocket probing depths (PPD) and gingival reces- cant for the purposes of the study.
sion (distance between cementoenamel junction and
gingival margin) were measured at the same six sites
per tooth as was BOP and the clinical attachment
Results
level (CAL) calculated as the sum of the PPD and
recession at each site. A site was considered peri- Tables and present the medical histories and drug
odontally affected when CAL was mm. A tooth regimens of the study DS population, respectively.
was considered periodontally affected when it had at The results of the present study are summarized in
least one site with CAL mm. A subject was diag- Tables .
nosed as suffering from periodontitis when at least Clinical examinations could not be performed on
one periodontally affected site was present. The mean four DS subjects due to lack of cooperation. In the
CAL, mean percentage of periodontally affected sites control group, radiographs were available for out
and mean percentage of periodontally affected teeth of the patients.
The Authors. Journal Compilation Blackwell Publishing Ltd
Journal of Intellectual Disability Research
495
Z. Maora et al. Outcome of a preventive dental programme on periodontal status in Downs syndrome

Table 1 Systemic diseases of Downs syndrome (DS) patients Table 2 Medications taken on a daily basis by Downs syndrome
(DS) patients

No. of DS suffering
Disease from disease (%) No. of DS subjects
Medication taking medication
(generic name) (%)
Hypothyroidism 15 (50)
Cataract 4 (13)
Congenital heart defects (total) 10 (33) Thyroxine 50/100/150 mcg 14 (46.6)
[defects that needs IE prophylaxis] [6 (20)] Hydroxocobalamin [Vit. B12] 4 (13.3)
Aortic valve insufficiency 4 (13.3) Furosemide 40 mg 1 (3.3)
Mitral valve prolapse 3 (10) Ferrous sulphate 2 (6.6)
Tricuspid valve insufficiency 1 (3.3) Famotidine 20 1 (3.3)
Atrial/ventricular septal defect 3 (10) Enalapril 5 mg 1 (3.3)
Chronic respiratory diseases 5 (16.6) Aspirin 100/75 mg 1 (3.3)
Anaemia (Vit. B12/Fe deficiency) 2 (6.6) Penicillin V 500 mg (prophylactic) 2 (6.6)
Psoriasis, arthritis, gout 2 (6.6) Valproic acid 200 mg 1 (3.3)
Hypertension 1 (3.3) Medroxyprogesterone acetate 500 mg 1 (3.3)
Eissenmenger syndrome 1 (3.3) Phenytoin 100 mg 1 (3.3)
Rheumatic heart disease 2 (5) Clotiapine 1 (3.3)
Epilepsy 1 (2.5) Clindium-Chlordiazepoxide 1 (3.3)
Thioridazine hydrochloride 25 mg 1 (3.3)
IE, infective endocarditis. Carbamazepine CR 400 1 (3.3)
Imipramine 50 mg 1 (3.3)

Table 3 Means of periodontal pocket depth (PPD), clinical attachment level (CAL) and percentages of periodontally affected subjects, sites
and teeth in Downs syndrome (DS) vs. controls

Controls DS P-value

PPD SD (n) 2.40 0.28 (28) 3.07 0.94 (26) 0.002*


CAL SD (n) 2.43 0.32 (28) 3.09 0.93 (26) 0.002*
Periodontally affected subjects 50 (14/28) 77 (20/26) 0.039
Periodontally affected sites SD (n) 3.64 5.60 (28) 14.83 21.73 (26) 0.006*
Periodontally affected teeth SD (n) 13.40 16.30 33.73 27.99 (26) 0.005*
(28)

*Wilcoxons test.

Chi-squared test.

Table 4 Mean percentage of periodontally affected teeth by tooth group in Downs syndrome (DS) vs. controls

Control (n) DS (n) P-value

Upper first molars SD 28.92 39.06 (28) 47.31 35.12 (26) 0.08
Upper central incisors SD 1.19 6.29 (28) 3.79 11.56 (26) 0.3
Lower first molars SD 17.73 32.83 (28) 17.31 18.69 (26) 0.27
Lower central incisors SD 2.22 11.54 (28) 8.50 17.99 (26) 0.03*

*Wilcoxons test.

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Journal of Intellectual Disability Research
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Z. Maora et al. Outcome of a preventive dental programme on periodontal status in Downs syndrome

Dental status only in the percentage of the periodontally affected


lower central incisors. The percentages of affected
In the DS group, (%) patients had lost at least
upper incisors and molars were greater in DS than in
one tooth due to periodontitis. Six patients were par-
controls, however, these differences were not statisti-
tially edentulous and one was completely edentulous.
cally significant. The percentage of affected lower first
These findings were significantly different from those
molars was similar in DS and controls (Table ).
found among individuals in the control group, who
Because the difference in the percentage of the
were fully dentate (P < .).
affected upper first molars between DS and controls
Mean plaque scores were similar in the study (DS)
was close to statistical significance (P = .), a fur-
and control (healthy) groups (.% vs. .%,
ther analysis was carried out which compared the
respectively, P = .).
number of patients without affected upper molars,
Mean BOP of the DS group was . times greater
with less than % and with more than % upper
than that of the control group, but this difference did
molars affected (Table ). The chi-squared test
not reach statistical significance (DS = . . vs.
revealed a significant increase (P = .) in the num-
controls = . ., P = .).
ber of the DS patients with affected upper molars
The most striking differences between the two
compared with the controls.
study groups were found in the measures of peri-
Table shows that the mean radiographic alveolar
odontitis. Table shows that the mean PPD, the
bone loss was significantly greater in DS subjects
mean CAL, the mean percentages of periodontally
compared with controls. Moreover, the percentages
affected patients, sites and teeth were significantly
of periodontally affected patients, sites and teeth, as
higher in DS compared with control group. When
calculated from the radiographs, were far greater in
classified according to the group of teeth involved,
DS subjects than in the controls. Figures and
the Wilcoxons test revealed significant differences
present two radiographs of DS patients with alveolar
bone loss around incisors and molars next to radio-
Table 5 Number of subjects with no periodontally affected upper graphs taken from identical sites of healthy age-
molars, % affected upper molars and % affected upper matched control.
first molars in Downs syndrome (DS) vs. controls
No statistically significant differences were found
between males and females for all the reported
No upper 150% of 51100% of parameters.
molars upper molars upper molars
affected affected affected

Discussion
Control 17 2 9
DS 7 7 12 This study assesses the periodontal status of a group
Total 24 9 21 of Israeli DS patients. When this group was examined
about years ago by Stabholz et al. (), the

Table 6 Mean radiographic bone loss (RBL) and mean percentages of subjects, sites and teeth with RBL in Downs syndrome (DS) vs.
control groups

Controls DS P-value

RBL SD (n) 1.50 0.42 (23) 2.56 0.87 (28) 0.0001*


% subjects 17.4 (4/23) 78.5 (22/28) <0.0001
% sites SD (n) 2.98 10.47 (23) 27.83 25.58 (28) 0.0001*
% teeth SD (n) 4.34 13.38 (23) 34.91 28.06 (28) 0.0001*

*Wilcoxons test.

Chi-squared test.

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Z. Maora et al. Outcome of a preventive dental programme on periodontal status in Downs syndrome

a b
b
Figure 2 Radiographs of incisor teeth of a healthy patient (a) vs. a
Downs syndrome (DS) patient (b). Arrows indicate severe alveolar
Figure 1 Radiographs of molar teeth of a healthy patient (a) vs. a
bone loss around the upper and lower incisor teeth.
Downs syndrome (DS) patient (b). Arrows indicate severe alveolar
bone loss on the mesial side of the first permanent molars.

adult DS patients in Greece. The degree of similarity


authors used the community periodontal index of is even more surprising, given that the control group
treatment needs (CPITN) to evaluate the periodontal was recruited from staff and students of the Faculty
status of the patients as well as their periodontal of Dental Medicine. This might well have incorpo-
treatment needs. Based on their recommendations, rated a bias towards a better oral health. This finding
this DS population was enrolled in a preventive den- further emphasizes the positive effect of the preven-
tal health programme which included periodical tive programme on the oral hygiene in these patients.
supragingival and subgingival de-plaquing and scal- Alternatively, it is possible that the plaque scoring
ing by a trained dental hygienist (Shapira & Stabholz technique used may not have been sufficiently sensi-
). The present study evaluated the long-term tive to identify possible existing differences between
consequences of this preventive programme and teeth with light and heavy plaque deposits.
attempted to evaluate clinically and radiographically In contrast to the similar oral hygiene and gingival
the periodontal status of this DS population and in conditions found in both study groups, the severity
addition, to compare their periodontal measures with of periodontitis among the DS population was signif-
those of healthy age-matched controls who were icantly greater than that of the control group. The
never exposed to such preventive programme. prevalence, extent and the severity of periodontitis
Similar plaque and gingival health measures were (measured clinically and radiographically) were
found in both the DS and control groups. This find- higher in the DS subjects. The fact that the differ-
ing is in contrast to previous studies that reported ences between the two study groups were more obvi-
lower levels of oral hygiene in institutionalized popu- ous radiographically than clinically, is probably due
lations (Cutress ; Vigild ), and is probably to an inevitable measuring inaccuracy during peri-
attributed to the long-term preventive dental pro- odontal probing in the DS less compliant individuals.
gramme which comprised the entire DS population. Moreover, when calculating the CAL and alveolar
These findings further extend those described by bone loss, the relatively large number of missing teeth
Shapira & Stabholz (), who reported their initial due to periodontal disease among DS patients under-
findings following only months of the preventive estimates the prevalence and severity of periodontitis
dental programme. Sakellari et al. () have also in this group.
found significant positive effects of professional Systemic diseases (diabetes mellitus, epilepsy, etc.)
supragingival cleaning and close monitoring of the and/or their pharmacotherapy (insulin, phenytoin,
oral hygiene habits on plaque and BOP indices in five calcium blockers, cyclosporin, etc.) might affect
The Authors. Journal Compilation Blackwell Publishing Ltd
Journal of Intellectual Disability Research
498
Z. Maora et al. Outcome of a preventive dental programme on periodontal status in Downs syndrome

the periodontal condition (Ciancio ; Meyle & alveolar bone loss assessment (Kallestal & Matsson
Gonzales ). In the present study, only one DS ; Akesson et al. ) particularly in the incisors
subject was taking phenytoin, and none suffered from region which is often more distorted than the poste-
a systemic disease that might affect periodontal sta- rior areas. Studies that compared periodontal status
tus. Fifteen DS patients suffered from hypothyroid- of DS individuals in the mixed dentition stage, might
ism and were taking hormone replacement therapy also be biased due to the significant delay in tooth
(Eltroxin, Glaxo Wellcome, Research Triangle Park, eruption compared with controls of the same age
NC, USA), which is not known to affect periodontal (Barnett et al. ; Desai ).
health. Thus, the deterioration in the periodontal sta- Cichon et al. () conducted an intervention
tus could not be attributed to systemic disease or study to determine the effectiveness of a -month
medication. supragingival plaque control and oral hygiene instruc-
In agreement with previous studies, the teeth most tions, in a group of young DS patients. They found
commonly and severely affected by periodontitis neither an improvement in the gingival condition nor
among our group of DS subjects were the lower central a reduction in the mean probing depth and the per-
incisors and the upper first molars. The susceptibility centage of periodontally affected sites. Another study
of these specific teeth to periodontitis might be asso- that investigated the results of a preventive pro-
ciated with the fact that these teeth are the first to gramme, examined DS patients who were recalled
erupt, thus being exposed for longer periods of time years after a baseline examination (Agholme et al.
to destructive factors (Cohen et al. ; Sznajder ). Significant increases in alveolar bone loss
et al. ; Cutress ; Saxen et al. ; Modeer (from % to %) and periodontitis prevalence
et al. ; Agholme et al. ). However, only (from % to %) were observed despite a marked
years separate the eruption of the severely affected improvement in the gingival condition. The authors
incisor and molar teeth from the far less affected suggested that the improved gingival condition might
canines, premolars and second molars. It would seem be due to the fact that more patients participated in
inappropriate to ascribe the stark difference in the preventive dental care at the follow-up compared with
periodontal condition of the latter teeth to their pres- baseline. However, the authors were unable to draw
ence in the mouth to this short time interval. any conclusions regarding the effectiveness of this
The present findings regarding the young age of programme because of lack of standardization of the
onset, the severe periodontal destruction and its typ- prophylactic treatment in all patients. The oral health
ical radiographic appearance as well as the typical prevention protocol of that study was similar to the
distribution of bone loss around specific teeth in the one used in our study population in terms of patients
present DS population is consistent with the disease age, teeth examined and methods employed. The
pattern of localized aggressive periodontitis and con- degree of alveolar bone loss and prevalence of peri-
firm the findings reported for other DS populations odontitis were similar in both studies.
(Cutress ; Saxen et al. ; Modeer et al. ; Based on our results, it is difficult to assess the
Agholme et al. ). effect of a dental preventive programme on the devel-
Comparing the present findings with the limited opment and progression of periodontitis because we
number of previously published epidemiological and are lacking baseline clinical and radiographic peri-
clinical studies on DS populations is problematic due odontal measurements. However, it seems that the
to different methods used in each of them regarding dental programme could not prevent the periodontal
indices, radiographic techniques and age groups destruction in the DS patients participating in this
involved. Most studies have used periodontal probing study. The clinical and radiographic parameters
depth and not CAL as a primary or a single clinical closely resemble those of localized aggressive peri-
parameter to define periodontitis (Modeer et al. odontitis where oral hygiene seems to play a minor
; Agholme et al. ). This might lead to erro- role in the pathogenesis of periodontitis.
neous conclusions disregarding gingival swelling Rather than looking for a local factor, the indica-
(which causes false pockets) and gingival recession. tions are that an immunological defect in DS patients
Other studies have used panoramic radiographs appears to be the cause of the rapid destruction of
which are less accurate than bite-wing X-rays for the periodontium. The long list of suspected predis-

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Journal of Intellectual Disability Research
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Z. Maora et al. Outcome of a preventive dental programme on periodontal status in Downs syndrome

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The Authors. Journal Compilation Blackwell Publishing Ltd

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