PERIODONTAL DISEASE IN P A T I E N T S W I T H D O W N S Y N D R O M E

Why is periodontal disease more

prevalent and more severe in people
with Down syndrome?
James Morgan, BA, BDentSc
Co. Kildare, Ireland. Corresponding author E-mail: morganjs@gmail.com

Spec Care Dentist 27(5): 196-201, 2007

Introduction
Down syndrome (DS) is an autosomal chromosomal disorder resulting from trisomy of
all or part of chromosome 21.’ Approximately 95% of people with DS have an extra
complete chromosome 21. The remaining 5% result from other chromosomal abnor-
malities including translocation in 3% of people and mosaicism in 2% of The
incidence of DS is generally cited as being between 1 in 600 to 1 in 1,000 live births.’
In Ireland, this condition affects approximately 1 in 580 live births, which is the high-
est incidence in E ~ r o p e . ~
Periodontal disease is defined as “an inflammatory disease of the supporting tissues
of the teeth caused by specific microorganisms, resulting in progressive destruction of
the periodontal ligament and alveolar bone with pocket formation, recession, or both.”’
The pathogenesis of periodontal disease is complex. In response to microbial sub-
stances released from plaque bacteria in the gingival sulcus, epithelial and connective
tissue cells are stimulated to produce inflammatory mediators, leading to infiltration
of the connective tissue by numerous defense cells. In the early stages of the immune
response, neutrophils predominate. As further microbial substances enter the sys-
temic circulation, committed lymphocytes return to the site of infection, and
antibodies specific to bacterial antigens are produced by plasma cells. This essentially
protective response is enough to control the infection in people who are not suscepti-
ble to periodontitk6

In susceptible individuals, however, In 2005, the World Health

the primary host defenses are unable to
control the microbial challenge, leading
to the epithelium becoming increasingly
permeable and ulcerated. There is
increased migration of neutrophils into
the tissues, which secrete a variety of
inflammatory mediators and proteolytic
enzymes. Once the concentration of
these inflammatory mediators and
enzymes becomes pathologically high,
~~S~Q~Q@ ht%\\\L~\Qi
L& Of tlhP t&agen
fibers, periodontal ligament, and alveolar
bone occurs.6 Preshaw et aL6noted that
the majority of periodontal destruction is
the result of “collateral damage arising
from the activation of the host defenses
against the presence of bacteria”.
Organization provided an overview of
periodontal disease worldwide and
reported that 10%to 15% of adults suf-
fered from periodontal d i ~ e a s eBrown
.~ et
al8reported that the prevalence of peri-
odontal disease among the general
population in the United States ranged
from 29% for persons aged 19 to 45
years, to 50% for persons aged 45 years
and older. An increased prevalence
severity of periodontal disease has been
reported in people with DS compared
with age-matched subjects of similar
levels of intellectual impairment and
compared with the general population?u
Prevalence varies between 58%and 96%
for those under 35 years of age.”

196 Spec Care Dentist 2 7 ( 5 ) 2007

 PERIODONTAL DISEASE I N PATIENTS WITH D O W N SYNDROME
The increased prevalence and severity
of periodontal disease in persons with
Down syndrome may be attributed to a
range of local factors associated with the
oral cavity, as well as systemic factors
associated with the genetic disorder itself.
Prevalence and severity of
periodontal disease
Johnson and YoungI4examined 70 chil-
dren with DS (mean age 10.8 +/- 3.0 years)
and compared them with 40 age-matched
subjects who did not have DS but had
similar learning disabilities. The presence
of periodontal disease was observed in
96% of persons in the group with DS and
it was much more severe than in the con-
trol group. Bone loss followed a horizontal
pattern and was most obvious in the lower
anterior segment. Agholme et al.,” Cichon
~ Saxen et al.” also observed this
et ~ l . , ’and
pattern of bone loss.
Saxen et al.” used orthopantomo-
grams to provide a more objective
method for evaluating periodontal dis-
ease. Bone loss was measured from the
cemento-enamel junction to the alveolar
bone margin. A tooth with bone loss of
5mm or more was regarded as affected. It
was reported that 69% of subjects with
DS aged 9 to 39 years had more than
5mm bone loss compared with 20% of
the control group, despite similar levels
of plaque and calculus. In a follow-up
study carried out five years later, the
prevalence of bone loss of 5mm or more
had increased to 75% in the subjects
with DS.l8
In a longitudinal study carried out by
Agholme et al.,” periapical and bitewing
radiographs were used to aid in the diag-
nosis of periodontal disease. It was
reported that 35% of subjects with DS
(mean age 16.6 years) had experienced
alveolar bone loss. Seven years later the
prevalence of alveolar bone loss had
increased to 74%.
C u t r e ~ sreported
’~ that persons with
DS who were living in institutions had
poorer levels of plaque control,
increased calculus deposits, and an
increased prevalence of periodontal dis-
ease when compared to subjects living at
home with DS. Swallowzocame to the
same conclusions.
Morgan
Etiology of periodontal
disease in Down syndrome
Local factors
Oral hygiene
Cohen et ~1.’’ studied a group of 100 sub-
jects with DS and found that oral
hygiene was generally poor. This was in
agreement with Sakellari et aI.ln who
reported that people with DS had poorer
oral hygiene than healthy individuals. In
another study, Sakellari et ~ 1 . found
’~ that
the mean plaque score was 100% in a
group of subjects with DS who were
between the ages of 26 and 37 years.
Sakellari2’also found that following oral
hygiene instruction, subjects with DS
had reduced ability to maintain adequate
plaque control. This could possibly be
associated with impairment of fine motor
function resulting in poor manual dex-
terity, as reported by Desai.’
Cohen et ~1.’’ reported that calculus
deposits were abundant among children
with Down syndrome. This was in agree-
ment with a similar study by Johnson
and Y ~ u n g . However,
’~ a less severe dis-~ 1 . observed
tribution of calculus was reported by
Barr-Agholme et ~ 1 (20%) . ~ and~ by Sasaki
et ~ 1 . (14.8%),
’~ respectively.
Open-mouth breathing
Persons with Down syndrome exhibit
characteristic phenotypical orofacial
anomalies including an underdeveloped
facial mid-third resulting in a hypoplastic ences, however, were found in relation to
maxilla and mandibular prognathism.’
The hypoplastic maxilla, combined with
an enlarged tonsillar volume, causes
upper airway congestion and a tendency
for increased mouth-breathing.’,’
Swallow” reported that 82.9% of children
with DS had their lips habitually apart.
Tooth morphology
Several authors have discovered irregu-
larities in the morphology of crowns and
roots in persons with DS.
Desai et al.’ reported that clinical
crowns were usually shorter and smaller
than normal in subjects with DS, and
that root length was reduced. Bajic et dZ5
reported a significant reduction in root
length as well as an increased prevalence
of fused molar roots in persons with DS.
The prevalence of fused molar roots in
the maxilla was 65.1%, and in the
mandible it was 40.5%, compared with
40.5% and 21.1%, respectively, in the
general population. C u t r e ~ salso
’ ~ sug-
gested that tooth morphology, including
short roots, could influence periodontal
disease in persons with Down syndrome.
Microbiological plaque
composition
Studies1n,’1.22,26-28
detailing the microbiolog-
ical composition of plaque from subjects
with DS vary in reporting different types
of organisms involved in the periopatho-
genic process. Sakellari et ~ 1 . reported
’~
that subjects with DS in all age groups
had significantly higher levels of peri-
odontopathic bacteria. In particular, a
significantly higher prevalence of P gingi-
valis, A. actinomycetemcomitans (A.u.), I:
forsythesis, and P intermedia was
observed. These findings suggest that
colonization by significant periodontal
pathogens occurs frequently in subjects
with DS, even in adolescence. Amano et
’~ that even in early child-
hood (age 2 to 4 years) significantly
higher levels of P gingivalis, B. forsythis,
and 1 denticola were detected in subjects
with DS. These are considered to be
important pathogens in severe types of
adult periodontitis.’6 In particular, the
occurrence of P gingivalis was found to
increase with age. No significant differ-
A.a. between subjects with DS and
healthy age-matched controls. Morinushi
et aLZ7measured the serum antibody titer
of subjects with DS to various periodon-
topathic bacteria and found that even in
subjects with DS under the age of 6
years, the average antibody titer to A.u.,
E nucleaturn, and P intermedia exceeded
that of the normal adult reference pool.
It was also found that these titers
increased significantly with age. These
findings suggest that A.u., E nucleatum,
and P intermedia are probably present in
significant numbers in subjects with DS,
even in those under the age of 6 years.
Hanookai et ~ 1 investigated
. ~ ~ the
prevalence of herpes virus species in
periodontally involved subgingival sites
in subjects with DS. It was found that
32% of patients had Epstein-Barr virus-1,
Spec Care Dentist 27(2) 2007 197
PERIODONTAL DISEASE I N PATIENTS WITH D O W N SYNDROME
26% human cytomegalovirus, and 16%
herpes simplex virus. Herpes virus
species may cause periodontal pathology
by suppressing the activity of B- and T-
lymphocytes as well as up-regulating
certain pro-inflammatory mediators such
as IL-1 and TNF-alpha.z8
Acute necrotizing ulcerative gingivitis
(ANUG)
Cohen et reported that of 100 sub-
jects with DS examined, 29% had
experienced ANUG. In a later study,
Brown et uL30compared 149 subjects
with DS with 657 normal subjects and
found that at least 35.6% of patients with
DS had experienced at least one episode
of ANUG compared with 4.1% of the
control group. Of the affected subjects
with DS, 49.1% had experienced recur-
rent episodes. The mean age at the time
of the first recorded episode was 9.4 +/-
4.4 years, even though ANUG typically
affects young Dissimilarities in
the diagnostic criteria for ANUG have
led to confusion in the literature as to its
prevalence among the general popula-
tion. These values range from less than
1% to 6.9%.32
Systemic factors
Neutrophil dysfunction
“Neutrophils are the primary cells
involved in the first line of host defense
against bacterial infe~tion.”~)
“Neutrophils have multiple surface
receptors that enable them to bind to and
phagocytize bacteria once they reach the
site of i n f e ~ t i o n . In
” ~ the
~ different stages
of periodontal disease, accumulation of
neutrophils in the connective tissue,
junctional epithelium, and gingival
sulcus are characteristic morphological
findings.35
Izumi et al.” reported that neutrophil
chemotaxis was significantly impaired in
subjects with DS when compared with
healthy controls. The authors found that
50% of subjects with DS had defective
neutrophil chemotaxis. They also found
that the prevalence of bone loss in sub-
jects with DS was inversely proportional
to the neutrophil chemotactic index of
the patient. These findings are in agree-
ment with Yavuzyilmaz et al.,35who
198 Spec Care Dentist 27(5) 2007
found a reduction in neutrophil chemo-
taxis, in neutrophil phagocytosis, and in
the mean random migration of neu-
trophils. The relatively short half-life of
neutrophils in people with DS (3.7 hours
compared with 6.6 hours in healthy indi-
viduals) may account for their neutrophil
dysf~nction.~~
T-lymphocyte dysfunction
Cichon et ~ 1 . reported
’~ that peripheral T-
lymphocytes in subjects with DS have a
diminished ability to recognize and
respond to specific antigens. This study
demonstrated a quantitative and qualita-
tive deficiency of T-lymphocytes.
Clee-Sohoel et ~ 1observed. ~ ~that the
number of T-cell receptor-bearing lym-
phocytes in marginal periodontitis in
subjects with DS was less than in other-
wise healthy individuals. Shaw and
Saxby3’stated that the percentage of cir-
culating T-cells is low from birth and
suggested that T-cell maturation may be
an integral part of Down syndrome.
Whittingham et ~ 1 demonstrated
. ~ ~ an
atypical immunodeficiency of the T-lym-
phocyte system. The authors reported
that the T-cell pattern included hypo-
responsiveness to antigenic stimulus, a
low mitotic activity, and an increase in
immature T-lymphocytes.
Bjorksten et ~ 1 . ’reported
~ a link
between depressed neutrophil chemo-
taxis and depressed lymphocyte
responsiveness in patients with DS who
had low serum zinc levels. Following a
two-month course of treatment with zinc
phosphate, an increase in serum zinc
levels as well as enhanced neutrophil and
T-lymphocyte function was observed.
Zinc is involved in numerous metabolic
pathways and is essential for synthesiz-
ing RNA and DNA.+O
Inflammatory mediators and proteolytic
enzymes
Komatsu et ul.+lfound that tissue
destruction related to progressive peri-
odontitis was due to actions of both the
host and bacterial-derived proteolytic
enzymes. Barr-Agholme et a1.4Lreported
that the mean level of Prostaglandin E2
(PGE2) in the gingival crevicular fluid
(GCF) of subjects with DS was signifi-
Periodontal disease In patients w i t h Down syndrome
cantly higher than in the healthy con-
trols. This finding was in agreement with
a similar study carried out by
Tsilingaridis et ~ 1 . PGE2
~ ’ was present in
inflamed periodontal tissue and was a
potent mediator of bone r e ~ o r p t i o n . ~ ~
Barr-Agholme et uL4*also proposed that
the enhanced levels of PGE2 found in
the GCF of patients with Down syn-
drome might be related to the altered
composition of the subgingival
microflora. This suggestion was based on
the fact that lipopolysaccharide from A.u.
has been reported to stimulate the pro-
duction of PGE2 in monocytes.42
Komatsu et ~ 1 reported
. ~ ~that the
production of matrix metalloproteinases
was significantly higher in subjects with
DS than in the control group. These find-
ings were in agreement with Tsilingaridis
et ~ l . “Matrix
+~ metalloproteinases com-
prise a family of proteolytic enzymes that
collectively degrade the extra-cellular
matrix in chronic inflammatory diseases
such as periodontitis.”’+
Hyper-innewation of the gingiva
Barr-Agholme et a1.” observed that the
gingivae of subjects with DS display pro-
found inflammatory reactions alongside
hyper-innervation of what was assumed
to be the sensory part of the innervation
of the gingiva. This “hyper-innervation”
may not be particular to Down syndrome
but may be a reaction brought on by
inflammation. Alternatively, chemical
transmitters released from these nerves
may be responsible for the inflammatory
reaction observed.+jThis phenomenon
may explain results obtained from two
studies on experimental gingivitis, which
showed that despite identical plaque
accumulation, the gingivae of subjects
with DS had more extensive inflamma-
tion when compared to age-matched
healthy i n d i v i d ~ a l s47. ~However,
~ func-
tional defects of neutrophils and
lymphocytes have also been proposed as
possible explanations for the difference
in gingival response to plaque.47
Barriers to dental services
Kaye et ~ l . reported
+~ that while most
adults with DS regularly attended their
dentist, little treatment was actually pro-
 PERIODONTAL DISEASE I N PATIENTS WITH D O W N SYNDROME
vided. Allison et al.+’observed that par-
ents of children with Down syndrome
frequently encounter problems with
access to oral care for their children.
Children with DS were significantly less
likely to receive dental treatment than
their non-DS siblings. Although some
authors16lR have reported that preventive
programs have little effect on the pro-
gression of periodontal disease in
patients with Down syndrome, more
recent studies924 have shown the effec-
tiveness of frequent preventive care.
Yoshihara et al.’ demonstrated the useful-
ness of periodic preventive care in
suppressing the severity and progression
of periodontal disease in subjects with
DS. In their study, patients were divided
into two groups: those who had received
frequent preventive care, and those who
had not been treated professionally in
more than a year. Significant reductions
were noted in mean pocket depth
(2.5mm and 3.lmm, respectively), mean
frequency of periodontal pockets (46%
and 91% respectively), and frequency of
the prevalence of pathological alveolar
bone loss (62% and 100% respectively),
when the “managed group” was com-
pared to the “interrupted group.” Sasaki
et al.24showed the efficacy of monthly
preventive care, which consisted of
mechanical plaque control and oral
hygiene instruction over a period of two
and a half years. Significant reduction in
gingival inflammation and probing
pocket depths were noted at that time
(mean pocket depth at baseline was
2.9mm and after 2.5 years was 1.3mm).
The use of chlorhexidine mouthwash to
compensate for ineffective plaque
removal has also been advocated.5@
Discussion
People with Down syndrome experience
more prevalent and severe periodontal
di~ease.~.’~
It has been r e p ~ r t e d ~that
~ . ~the
’ decrease in neutrophil function might
progression of the disease in persons with
DS was similar to aggressive periodontal
disease. A multi-factorial etiology
accounting for this prevalence and sever-
ity has been proposed. People with DS
have poorer levels of oral hygiene,2,1@,21,22 syndrome), an increase in periodontal
and increased c ~ ~ c u ~ However. u s . ~ ~ ~ disease
Morgan
most authors agree that the amount of
plaque and calculus present was not com-
mensurate with the severity of
periodontal disease observed. Lh~17,L9,21,47,51
Open-mouth breathing reduces the
cleansing action of the saliva and encour-
ages the accumulation of plaque; it also
dehydrates the gingival tissues, which
may impair the individual’s resistance to
i n f e ~ t i o nShorter
.~~ root lengths and an
increased prevalence of fused roots may
also influence periodontal d i ~ e a s eIt. ~ ~ ~tant
has been suggested that the fused molar
roots favor the progression of periodontal
disease because occlusal forces have a
greater effect on these than on teeth with
divergent
Subgingival plaque in people with DS
harbors increased amounts of suspected
periodontal pathogens.1@.26-28 Gram-nega-
tive bacteria contain lipopolysaccharide
in their cell wall. Among other effects,
lipopolysaccharide has the potential to
activate the complement system, produce
inflammation, and stimulate bone resorp-
t i ~ nHerpes
. ~ ~ virus can also influence
periodontal disease. Hanookai et a1.28
suggested that periodontal herpes virus
and bacterial co-infections might favor
destructive periodontal disease. However,
few studies have been carried out on this
subject.
ANUG is more prevalent in Down
s y n d r ~ m e . ’ANUG
~ . ~ ~ can result in the
formation of characteristic gingival
craters, which encourages plaque stagna-
tion, and can favor the progression of
any underlying periodontal
Neutrophils and T-lymphocyte func-
tion is impaired in people with DS.16,33.35,36in slowing the progression and reducing
Neutrophils play an intimate role in the
periodontal disease process because they
have the ability to detect and migrate
toward infection and phagocytose
microorganism^.'^ Van Dyke et ~ 1 sug- . ~ ~ their oral health. Fiske and Shafik’ rec-
gested that because of this close
involvement in periodontal disease, a
result in more severe periodontal break-
down. They also suggested that in
diseases where neutrophil function was
impaired (for example, neutropenia,
Papillon-Lefevre syndrome, and Down
~ ~ ~was ~ usually
~ ~ ~ seen.54
~ ~ The
~ + immune
system can be further compromised by
the T-cell dysfunction in Down syn-
drome. Whittingham et al.3Rproposed
that the T-cell dysfunction “might be
explained by failing immuno-competence
due to accelerated ageing”. He further
proposed that it might even be caused
“by a heavy load of infections early in life
because of an incapacity to maintain ade-
quate standards of personal hygiene”.
Preshaw et aL6highlighted the impor-
~ ~role
~ ~ played by both inflammatory
mediators and proteolytic enzymes in the
pathogenesis of periodontal disease. Both
PGE2 and matrix metalloproteinases
have been shown to be present in signifi-
cantly higher levels in people with DS.4143
PGE2 is a vasodilator, which is “involved
in the increased vascular permeability
occurring at sites of inflammation, and a
mediator of bone demineralization” .44
Matrix metalloproteinases can degrade
type I-V collagens, laminin, gelatin,
fibronectin, and elastin.44
Institutionalization has been
~hown’’.~@ to be associated with an
increased prevalence and severity of peri-
odontal disease. Swallow*@ proposed that
this may be a reflection of the quality of
oral hygiene practiced, whereby aid given
to non-institutionalized children by their
parents may slow the disease’s process.
Cutress’’ suggested that fecal-oral trans-
mission of contagious microorganisms in
institutionalized patients may account
for the increased prevalence of periodon-
tal disease.
Recent s t ~ d i e s ’ have
~ ~ ~ reported
~~+ the
effectiveness of frequent preventive care
the severity of periodontal disease.
Therefore, any barriers that hinder the
access of people with DS to dental serv-
ices could have detrimental effects on
ommended the development and
instigation of a realistic preventive pro-
gram that would include regular scaling
and root planing, and advice regarding
anti-microbial agents. The results
obtained by Yoshihara et al.’ suggest that
to combat the severity and progression of
periodontal disease in persons with DS, a
more frequent treatment interval than
the six months suggested by Hennequin
Spec Care Dentist 27(5) 2007 199
 PERIODONTAL DISEASE IN PATIENTS WITH D O W N SYNDROME
et al.’ should be employed. In their study,
the mean interval between dental visits
in the managed group was 3.7 (+/- 1.3
months). Sakellari et al.L1also recom-
mended a three-month treatment
interval. It has been suggested that an
oral hygiene regime that includes
chlorhexidine - as a mouthwash, a gel,
or as a professionally applied varnish -
may be beneficial in reducing oral
plaque, and may help compensate for
inadequate t o o t h - b r ~ s h i n g . ~ ~
Conclusions
The increased prevalence and severity of
periodontal disease in persons with Down
syndrome is due partly to an inability to
adequately maintain oral hygiene. Other
contributing factors include an earlier
and more extensive colonization with
known periodontal pathogens along with
other local factors such as open-mouth
breathing, tooth morphology, altered
microbial plaque composition, and acute
necrotizing ulcerative gingivitis.
Increasing evidence, however, supports
the theory that an impaired immunity
due to a reduction in neutrophil chemo-
taxis, neutrophil phagocytosis, and
T-lymphocyte function, as well as an
increased production of inflammatory
mediators and proteolytic enzymes, may
contribute most to the prevalence and
severity of periodontal disease in persons
with Down syndrome.
Down syndrome is the most com-
monly diagnosed intellectual disability in
Ireland.4 In recent years, trends toward
de-institutionalizing people with Down
syndrome and placing them in commu-
nity settings have emerged.15Therefore, it
is increasingly likely that most dental
practitioners will encounter a patient
with Down syndrome. Every effort must
be made to encourage the implementa-
tion of frequent preventive care in order
to decrease the severity and progression
of periodontal disease in their patients.
Acknowledgements
The author acknowledges Prof. June
Nunn for her advice and encouragement
in writing this article.
200 Spec Care Dentist 2 7 ( 5 ) 2 0 0 7
References 16. Cichon P, Crawford L, Grimm WD. Early-
onset periodontitis associated with Down’s
1. Hennequin M, Faulks D, Veyrune JL,
syndrome-clinical interventional study.
Bourdiol P: Significance of oral health in per-
Ann Periodontol 1998; 3:370-80.
sons with Down syndrome: a literature
17. Saxen L,Aula S, Westermarak T. Periodontal
review. Dev Med Child Neurol 1999; 41:275-
disease associated with Down’s syndrome:
83.
an orthopantomographic evaluation. J
2. Desai S. Down syndrome: A review of the
Periodontol 1977; 48:337-41.
literature. Oral Surg Oral Med Oral Pathol
18. Saxen L,Aula S. Periodontal bone loss in
Oral Radio1 Endod 1997; 84:279-85.
patients with Down’s syndrome: a follow-up
3. Fiske J, Shafik H. Down’s syndrome and
study.] Periodontol 1982; 53:158-62.
Oral Care. Dent Update 2001; 28:148-56.
19. Cutress TW. Periodontal disease and oral
4. Bradley C, McAlister T. The oral health of
hygiene in trisomy 21. Arch Oral Biol 1971;
children with Down syndrome in Ireland.
16:1345-55.
Spec Care Dentist 2004; 24:55-60.
5. Newman MG, Takei H, Carranza FA.
20. Swallow JN.Dental disease in children with
Down’s syndrome. J Ment Defic Res 1964; 53
Carmnzak Clinical Periodontology, 9th ed.
Suppl: 102-18.
Philadelphia: Saunders; 1996: 67.
21. Cohen M, Winer RA, Shklar G. Periodontal
6. Preshaw PM, Seymour RA, Heasman PA.
disease in a group of mentally subnormal
Current concepts in periodontal pathogene-
children. J Dent Res 1960; 39:745.
sis. Dent Update 2004; 31:570-8.
22. Sakellari D, Belibasakis G, Chadjipadelis T,
7. Peterson PE, Ogawa H. Strengthening the
Arapostathis K, Konstantinidis A.
prevention of periodontal disease: the WHO
Supragingival and subgingival microbiota of
approach. J Periodontol 2005; 76:2187-93.
adult patients with Down’s syndrome.
8. Brown LJ,Oliver RC, Loe H. Periodontal
Changes after periodontal treatment. Oral
Diseases in the U.S. in 1981: Prevalence,
Microbiol Immunol 2001; 16:376-82.
severity, extent, and role in tooth mortality. J
23. Barr-Agholme M, Dahllof G, Modeer T,
Periodontol 1989; 60:363-80.
Engstrom P, Engstrom G. Periodontal condi-
9. Yoshihara T, Morinushi T, Kinjyo S,
tions and salivary immunoglobulins in
Yamasaki Y. Effect of periodic preventative
individuals with Down syndrome. J Periontol
care on the progression of periodontal dis-
1998; 69:1119-23.
ease in young adults with Down’s syndrome.
24. Sasaki Y, Sumi Y, Miyazaki Y, Hamachi T,
J Clin Periodontol 2005; 32556.60.
Nakata M. Periodontal management of an
10 Sakellari D, Arapostathis KN, Konstantinidis
adolescent with Down’s syndrome-a case
A. Periodontal conditions and subgingival
report. Int J Paediatr Dent 2004; 14:127-35.
microflora in Down syndrome patients. A
25. Bagic I, Verzak Z, Cukovic-Cavka S, Brkic
case control study.] Clin Periodontol 2005;
H, Susic M. Periodontal conditions in indi-
32:684-90.
viduals with Down’s syndrome, Coll Antropol
1 Amano A, Kishima T, Akiyama S, Nakagawa
2003; 27 Suppl 2:75-82.
I, Hamada S, Morisaki I. Relationship of
26. Amano A, Kishima T, Kimura S, et al.
periodontopathic bacteria with early-onset
Periodontopathic bacteria in children with
periodontitis in Down’s syndrome. J
Down syndrome. J Periodontol 2000; 71:249-
Periodontol 2001; 72:368-73.
55.
12 Agholme MB, Dahllof G, Modeer T. Changes
27. Morinushi T, Lopatin D, Van Poperin N. The
of periodontal status in patients with Down
relationship between gingivitis and the
syndrome during a 7-year period. Eur J Oral
serum antibodies to the microbiota associ-
Sci 1999; 107:82-8.
ated with periodontal disease in children
13 Orner G. Periodontal disease among chil-
with Down’s syndrome. J Periodontol 1997;
dren with Down’s syndrome and their
68:626-31.
siblings. J Dent Res 1976; 55:778-82.
28. Hanookai D, Nowzari H, Contreras A,
14 Johnson NP, Young MA. Periodontal disease
Morrison J, Slots J. Herpesvirus and peri-
in mongols. J Periodontol 1963; 34:41-7.
15 Barnett M, Press K, Friedman D, Sonnenberg
odontopathic bacteria in Trisomy 21
periodontitis. J Periodontol 2000; 71:376-84.
E. The prevalence of periodontitis and
29. Cohen M, Winer RA, Schwartz S, Shklar G.
dental caries in a Down’s syndrome popula-
Oral aspects of mongolism. Part 1.
tion. J Periodontal 1986; 57:288-93.
Periodontal disease in patients w i t h Down syndrome
 PERIODONTAL DISEASE I N PATIENTS WITH D O W N SYNDROME
Periodontal disease in mongolism. Oral Surg
Oral Med Oral Pathol 1961; 14:92-107.
30. Brown RH. Necrotizing ulcerative gingivitis
in mongoloid and non-mongoloid retarded
individuals.J Periodontal Res 1973; 8:290-5.
31. Eley BM, Manson JD. Periodontics. 5th ed.
Chapter 25. Acute necrotizing ulcerative
gingivitis. Wright; 2004: 354-7.
32. Falkler WA, Martin SA, Vincent JW, Tall BD,
Nauman RK, Suzuki JB. A clinical, demo-
graphic and microbiologic study of ANUG
patients in an urban dental school. J Clin
Periodontol 1987; 14:307-14.
3 Izumi Y,Sugiyama S, Shinozuka 0,
Yamazaki T, Ohyama T, Ishikawa I.
Defective neutrophil chemotaxis in Down’s
syndrome patients and its relationship to
periodontal destruction. J Periodontol 1989;
60:238-42.
34. Deas DE, Mackey SA, McDonnell HT.
Systemic disease and periodontitis: manifes-
tations of neutrophil dysfunction.
Periodontol2000 2003; 32;82-104.
35. Yavuzyilmaz E, Ersoy F, Sanal 0, Tezcan I,
Ercal D. Neutrophil chemotaxis and peri-
odontal status in Down’s syndrome patients.
J Nihon Univ Sch Dent 1993; 35:91-5.
36. Sohoel DC, Jonsson R, Johannessen AC,
Nilsen R. Gammddelta T lymphocytes in
marginal periodontitis in patients with
Down’s syndrome. Adv Exy Med Biol 1995;
371Bz1135-6.
37. Shaw L, Saxby MS. Periodontal destruction
in Down’s syndrome and in juvenile peri-
Morgan
odontitis. How close a similarity?J
Periodontol 1986; 57:709-15.
38. Whittingham S, Pitt DB, Sharma DL,
Mackay IR. Stress deficiency of the T-lym-
phocyte system exemplified by Down
syndrome. Lancet 1977; 1:163-6.
39. Bjorksten B, Back 0, Gustavson KH,
Hallmans G, Hagglof B, Tarnvik A. Zinc and
immune function in Down’s syndrome. Acta
Paediatr Scand 1980; 69:183-7.
40. Kumar P, Clark M. Clinical Medicine. 6th ed.
Edinburgh: Elsevier Ltd; 2005:249.
41. Komatsu T, Kubota E, Sakai N.
Enhancement of matrix metalloproteinase
(MMP)-2 activity in gingival tissue and cul-
tured fibroblasts from Down’s syndrome
patients. Oral Dis 2001; 7:47-55.
42. Barr-Agholme M, Krekmanova L, Yucel-
Lindberg T, Shinoda K, Modeer T.
Prostaglandin E2 level in gingival crevicular
fluid from patients with Down syndrome.
Acta Odontol Scand 1997; 55:101-5.
43. Tsihngaydis G ,Yuce\LindbtxgT ,Modtey T .
Enhanced levels of prostaglandin E2,
leukotriene B4, and matrix metallopro-
teinase-9 in gingival crevicular fluid from
patients with Down Syndrome. Acta Odontol
Scand 2003; 61:154-8.
44. Page RC. The role of inflammatory media-
tors in the pathogenesis of periodontal
disease. J Periodont Res 1991; 26:230-42.
45. Barr-Agholme M, Modeer T, Luthman J.
Immunohistological study of neuronal
markers in inflamed gingiva obtained from
children with Down’s syndrome. J Clin
Periodontol 1991; 18:624-33.
46. Reuland-Bosma W, Liem RS, Jansen HW, van
Dijk LJ, van der Weele LT. Morphological
aspects of the gingiva in children with
Down’s syndrome during experimental gin-
givitis. J Clin Periodontol 1988; 15:293-302.
47. Reuland-Bosma W, van Dijk LJ, van der
Weele L. Experimental gingivitis around
deciduous teeth in children with Down’s
syndrome. J Clin Periodontol 1986; 13:294-
300.
48. Kaye PL, Fiske J , Bower EJ, Newton JT,
Fenlon M. Views and experiences of parents
and siblings of adults with Down syndrome
regarding oral healthcare: A qualitative and
quantitative study. Br DentJ 2005; 198:571-8.
49. Allison PJ, Hennequin M, Faulks D. Dental
care access among individuals with Down
syndrome in France. Spec Care Dentist 2000;
20:28-34.
50. Nunn J. Disability and Oral Care. London:
F D \ W ~ YDenla\
\ ~ Press: 200Q33.
51. Reuland-Bosma W, van Dijk LJ. Periodontal
disease in Down’s syndrome: A review. J Clin
Periodontol 1986; 13:64-73.
52. Eley BM, Manson JD. Periodontics. 5th ed.
Edinburgh: Elsevier Ltd; 2004: 43.
53. Eley BM, Manson JD. Periodontics. 5th ed.
Edinburgh: Elsevier Ltd, 2004: 66.
54. Van Dyke TE, Levine MJ, Genco RJ.
Neutrophil function and oral disease. J Oral
Pathol 1985; 14:95-120.
S p e c C a r e Dentist 27(5) 2007 201