51

Role of periodontitis in hospital-acquired pneumonia

M.M. El Attar,
1
M.Z. Zaghloul
2
and H.S. El Menoufy
3
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ABSTRACT This study evaluated the role oI periodontal pathogens in 50 hospitalized patients with hospital-
acquired pneumonia compared with 30 healthy controls. Specimens oI oropharyngeal aspirate, dental plaque,
bronchoalveolar lavage and blood cultured 1 or more pathogens in around 80 oI patients, predominately
Staphylococcus aureus, Iollowed by coagulase-negative staphylococci, Streptococcus pneumoniae and Klesiella
pneumoniae. Antibiotic sensitivity patterns showed concordance oI bacterial cultures Irom dental plaque and
oropharyngeal cavity in 13 patients. C-reactive protein (CRP) levels were signiIicantly higher in patients than in
controls and there was a signiIicant correlation between serum and salivary CRP levels. Dental plaque bioIilm
may promote oral and oropharyngeal colonization oI respiratory pathogens in hospitalized subects.
R6le de la parodontite dans la pneumonie nosocomiale
RS Cette tude valuait le rle des agents pathognes priodontiques chez 50 patients hospitaliss
souIIrant de pneumonies nosocomiales compars un groupe de contrle comprenant 30 individus sains. Des
chantillons daspiration oropharynge, de plaque dentaire, de lavage broncho-alvolaire et de sang mis en
culture ont Iait apparatre un ou plusieurs agents pathognes chez environ 80 des patients, essentiellement
le Staphylococcus aureus, suivi par des staphylocoques coagulase ngative, le Streptococcus pneumoniae et la
Klesiella pneumoniae. es schmas de sensibilit au antibiotiques ont montr une concordance au niveau
des cultures bactriennes issues de la plaque dentaire et de la cavit oropharynge chez 13 patients. es tau
de protine C ractive taient nettement plus levs chez les patients que dans le groupe de contrle et une
corrlation importante a t observe entre les tau de protine C ractive sriques et salivaires. e bioIilm
constitu par la plaque dentaire peut Iavoriser la colonisation orale et oropharynge par des agents pathognes
respiratoires chez les suets hospitaliss.
1
!epartment of "hest !iseases#
2
!epartment of "linical $athology, %aculty of Medicine, Ain Shams &ni'ersity, "airo, Egypt ("orrespondence to
M.M. El Attar) may*el*a ttar+yahoo. c om,.
3
!epartment of -ral Medicine, $eridontology and !iagnosis, %aculty of !entistry, %uture &ni'ersity, "airo, Egypt.
Received 10508 accepted 1008
5
ol. 1 o. 5 010 astern editerranean ealth ournal
a Revue de Sant de la diterrane orientale
7ntroduction
There has been a recent resurgence
oI interest in the relationship between
oral health and a number oI
prevalent sys- temic diseases 1.3.
vidence in the last decade has
suggested that inIections oI the oral
cavity, especially periodontitis, are a ris
Iactor Ior pneumonia and other
respiratory diseases /. n the case
oI nosocomial or hospital-acquired
pneu- monia (AP) aspiration oI oral
bacteria during mechanical
ventilation is one possible route Ior
contamination oI the lower airways by
microorganisms /.0. t seems
logical, thereIore, to evaluate the role
oI dental plaque as a source oI these
bacteria, especially in patients with
periodontal disease 1,2. n general, the
bacterial proIile oI pneumonia in
non- ventilated hospital patients is
similar to that oI ventilated patients,
involving multidrug-resistant
pathogens such as methicillin-
resistant Staphylococcus au3 reus,
$seudomonas aeruginosa, Enteroacter
species and Klesiella pneumoniae 4.
Periodontitis is a chronic
inIlam- matory reaction to a speciIic
group oI bacteria that results in
destruction oI the supporting
connective tissue and bone oI the
tooth structure 15. t is a common
oral inIection that can aIIect the
hosts susceptibility to systemic dis-
ease in a number oI ways Ior
eample via shared ris Iactors such
as tobacco smoing, ageing and stress
via subgingi- val plaque bioIilms acting
as a reservoir oI ram-negative
anaerobic bacteria which are the main
pathogens in AP and via gingival
crevicular Iluid that contains
important bioactive molecules such as
enzymes and cytoines that may pass
into the saliva and be aspirated
2,11. C-reactive protein (CRP) levels
are an indicator oI host response
that reIlects periodontal destruction.
The aim oI this study in gypt was to
evaluate the role oI periodontal bacteria
in the pathogenesis oI AP
in high- ris patients by
eamining cultures and CRP
levels oI patients suIIering
Irom AP and periodontitis.
8ethods
9ample
The study group was 50 patients with
conIirmed AP who were suIIering Irom
moderate to severe chronic perio- dontitis.
AP was deIined as pneumonia occurring 8
hours aIter hospitalization and was
conIirmed by an increase in leuocyte
counts in addition to the clini- cal picture.
There were 3 males and 11 Iemales, age
range 50 years, mean age 50.5
standard deviation (SD) 8. years. The
study was carried out in the respiratory
intensive care unit oI Ain Shams
niversity ospitals, Cairo, over the period
anuary to December 00.
A group oI 30 apparently healthy
subects (5 males and 5 Iemales) were
recruited as a control group they were
relatives oI the patients. Their ages
ranged Irom 3 to 5 years, mean .8
(SD .) years.
The eclusion criteria Ior patients and
controls were nown systemic disease
history andor presence oI inIections
other than respiratory tract inIection or
periodontitis treatment with any
medication that might aIIect serum levels
oI inIlammatory marers pregnant or
lactating women and cur- rent smoers.
:ata collection
edical, dental and social history was
collected Irom both patient and control
groups and their systemic condition was
assessed according to the modi- Iied
Cornell edical nde 12. Both patients
and controls gave written in- Iormed
consent to participate there were no
reIusals. AIter giving consent all the
patients were subected to the Iollowing
Iull medical history taing and physical
eamination plain chest -ray
electrocardiogram liver and idney
Iunction tests and Iasting and
postprandial blood glucose level.
$eriodontal assessment
Periodontal assessment oI patients
and controls was carried out by at each
53



standing tooth, including gingival inde
13, plaque inde 1/, probing pocet
depth and clinical attachment level. The
control subects were selected to be Iree
Irom chronic periodontitis, which
was conIirmed by the absence oI
attach- ment loss, and the presence oI
probing depth _ 3 mm and gingival
inde 1 at all surIaces. Periodontal
assessments were done by the same
dentistperi- odontologist.
Probing depth and clinical attach-
ment levels were measured to the near-
est mm at sites on each tooth
using Williams graduated periodontal
probe. Both probing depth and clinical
attach- ment level scores around
each tooth were totalled and divided by
to obtain the score Ior this tooth. The
inde score per subect was then
obtained, by total- ling the scores oI
all teeth and dividing this by the
number oI teeth eamined.
The severity oI the periodontal con-
dition was characterized on the basis oI
the amount oI clinical attachment
loss, with moderate periodontitis
deIined as teeth sites ehibiting _ 3
mm and 5 mm clinical attachment
loss and severe periodontitis as teeth
sites with attach- ment loss _ 5 mm
16. ach subect had at least 0
standing teeth, none oI which had
untreated periapical lesions 10,11.
Specimen collection
Oropharyngeal aspirate (OPA)
swabs were collected Irom patients
and con- trols using an appropriate
wash into sterile tubes Ior
immediate culture. Bronchoalveolar
lavage (BA) speci- mens were
obtained Irom patients by Iiberoptic
bronchoscope (Olympus, Toyo,
apan) according to the recom- mended
guidelines 12. A portion oI the
specimens was send to the labora-
tory Ior quantitative culture within
1 hour oI collection. Whole
unstimulated specimens oI saliva were
obtained Irom patients and controls
and stored as aliquots at 0 C
Ior CRP determi- nation. A sample
oI m blood Irom patients and
controls was collected into
vacutainer tubes, centriIuged and the se-
rum was separated and stored at 0 C
Ior estimation oI CRP level. Another
3 m blood sample was collected
Irom the patients and inoculated into
Bactec Ped Plus blood culture vials
(Becton- Dicinson, SA) Ior
culture. Samples oI supra- and
subgingival dental plaque were
collected Irom the patients us- ing
appropriate wash and periodontal
curette. The specimens were placed in 1
m broth and transIerred to the labora-
tory within 1 hour.
7ests
icrobiological eamination oI
OPA, BA and plaque specimens
were done Irom ram-stained
smears Ior detec- tion oI pus cells
and microorganisms. Specimens
were cultured on blood agar,
acConey agar, chocolate agar and
Sabouraud detrose agar media. All
isolates were identiIied by colony
morphology and a set oI
biochemical tests 14. Quantitative
cultures oI BA were done using 10
colony-Iorming units (CF)m
as a cut-oII point Ior interpreting
BA cultures 25. For blood
cultures, the blood samples were
inoculated into vials which were
inserted into the BACTC Iluorescent
series instrument Ior incubation.
Sub- culture was done Irom positive
culture vials using blood agar,
acConey and chocolate agar media.
Antimicrobial susceptibility
testing (antibiogram) was
perIormed by the dis diIIusion
(KirbyBauer) method on similar
pathogens to those isolated Irom
patients specimens.
CRP level was determined in serum
and saliva oI both patient and
control groups by an enzyme-lined
immuno- sorbent assay (SA) it
(Cliniab, Cairo, gypt) according
to the manu- Iacturers instructions.
9tatistical anal;sis
Data were collected, tabulated and ana-
lysed using the S$SS, version 10.
Results
This study was carried on 50
patients with AP (3 males and
11 Iemales) and 30 controls (5
males and 5 Ie- males).
8icro<iolo=ical assessment
From the control group, OPA
cultures yielded only growth oI
normal upper respiratory tract Ilora,
and blood cul- tures yielded no
growths aIter to 10 days
incubation.
OI the 50 patients with AP, OPA
specimens Irom (8.0)
patients yielded growth oI
pathogens and 8 (1. 0) growth
oI normal upper
respiratory tract Ilora. The maority
oI the isolates were Sta. aureus
(3.8), Iollowed by coagulase-
negative staphy- lococci (1.0) and
Str. pneumoniae (1.) (Table 1).
Dental plaque specimens oI
(88.0) patients yielded growth
oI 1 or more pathogens Sta. aureus
(31.5) accounted Ior the maority
oI the 5 isolates, Iollowed by
8acteroids spp. (1.8), Str.
pneumoniae (1.8) and coagulase-
negative staphylococci (13.0) (Table
1).
All the BA specimens oI our
50 AP patients yielded growth oI
patho- gens. Sta. aureus (.8) were
cultured in the highest proportion oI
the 5 iso- lates, Iollowed by
coagulase-negative staphylococci
(1.3), K. pneumoniae (1.) and
Str. pneumoniae (10.) (Table 1).
The blood culture results
revealed that 3 (8.0) out oI
the 50 AP patients were positive
Ior pathogens. The isolated
organisms were predomi- nately Sta.
aureus (30.8), Iollowed by
coagulase-negative staphylococci
(1.8), Str. pneumoniae (10.3) and K.
pneumoniae (10.3) (Table 1).
n 10 (0.0) patients the
same organism (Sta. aureus) was
isolated Irom all body sites OPA,
dental plaque, BA and blood
specimens. The iso- lated
organisms displayed the same
>a<le ? @atho=ens isolated from orophar;n=eal aspirate AB@CDE dental plaqueE <ronchoalFeolar laFa=e AGCHD and
<lood specimens of patients Iith hospital-acquired pneumonia
@atho=en Brophar;n=eal
aspirate
An = JK culturesD
:ental plaque
An = LJ culturesD
Groncho-alFeolar
laFa=e
An = LM culturesD
Glood
An = NO culturesD
PoQ R PoQ R PoQ R PoQ R
Staphylococcus aureus 10 3.8 1 31.5 15 .8 1 30.8
Coagulase-negative staphylococci 8 1.0 13.0 8 1.3 5 1.8
Streptococcus pneumoniae 1. 8 1.8 10. 10.3
Klesiella pneumoniae 5 11. . 8 1.3 10.3
Escherichia coli .5 8 1.8 5 8. 3 .
$seudomonas aeruginosa .8 0 0.0 3 5. 5.1
Streptococcus pyogenes 3 .1 5 .3 .1 3 .
$eptostreptococcus 3 .1 5 .3 0 0.0 0 0.0
8acteroides spp. 0 0.0 8 1.8 3 5. 3 .
Haemophilus influen9ae 0 0.0 0 0.0 .1 3 .
>a<le K Cntimicro<ial suscepti<ilit; profile of the Staphylococcus aureus isolated from orophar;n=eal aspirate AB@CDE dental
plaqueE <ronchoalFeolar laFa=e AGCHD and <lood specimens of ?S patients Iith hospital-acquired pneumonia
@atho=enTspecimen
t;pe
Sta. aureus
BUacillin Vancom;cin CmpicillinT
sul<actam
PoQ of resistant isolates
Wr;throm;cin 8aUipim XiprofloUacin Yentamicin 7mipinam
OPA 0 0 3 3 3
Plaque 0 0 3 3 3
BA 0 0 3 3 3
Blood 0 0 3 3 3
antimicrobial susceptibility proIile Irom
all sites (Table ). n 3 (.0) patients
the same organisms were Iound in
3 body sites OPA, dental plaque
and BA specimens. These were
coagulase- negative staphylococci (1
patient), Str. pneumoniae (1 patient)
and K. pneumo3 niae (1 patient).
The isolated organ- isms displayed
the same antimicrobial susceptibility
proIile (Table 3).
9erolo=ical assessment
The age, serum CRP and salivary
CRP levels oI AP patients and
controls are shown in Table . ean
CRP levels in serum and saliva oI
50 AP patients 8. (SD 1.0)
gm and 11. (SD
.) gm respectively were
signiIi- cantly higher than those in
the controls .8 (SD 1.1) gm
and 1. (SD 0.8)
gm respectively. The
diIIerence between AP patients and
controls with regard to serum CRP and
saliva CRP was highly signiIicant (

0.33, $ 0.001).
There was signiIicant correlation be-
tween serum CRP and saliva CRP in
the AP patients (r 0.8) and
controls (r
0.0) using Pearson correlation coeI-
Iicient and by linear regression
curve (Figure 1).
:iscussion
t has been suggested that dental plaque
may act as a reservoir oI
respiratory pathogens, especially in
patients with periodontal disease 21.
One or more pathogens were
cul- tured Irom 88.0 oI the dental
plaque specimens oI AP patients.
Sta. aureus
accounted Ior the maority oI the
iso- lates, Iollowed by 8acteroides
spp., Str. pneumoniae and coagulase-
negative sta- phylococci. Russell et al.
reported that Sta. aureus and ram-
negative bacilli (E. coli and E. cloacae)
and $. aeruginosa were the predominant
respiratory pathogens
Respiratory inIection is thought to rely
in part on the aspiration oI
oropharyngeal Ilora into the lower respiratory tract and Iailure oI the host deIence
mechanisms to eliminate the contaminating bacteria, which then multiply to
cause inIection.
Zi=ure ? Hinear re=ression curFe of serum and saliFa X-reactiFe protein AXR@D
leFels in AaD patients Iith hospital-acquired pneumonia An = LSD and A<D controls
An = NSD
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isolated Irom the dental plaque oI

institu- tionalized elderly people 22. All oI
the BA specimens Irom our 50 AP
patients yielded growth oI 1 or
pathogens, predominantly Sta. aureus,
coagulase-negative staphyloco- cci, K.
pneumoniae and Str. pneumoniae. The great
maority oI OPA specimens Irom AP
patients (8.0) also yielded growths
oI pathogens mainly Sta. aureus,
coagulase- negative staphylococci and Str.
pneumoniae. Scannapieco et al. reported that
poor oral hy- giene and periodontal disease
may promote oropharyngeal colonization
by potential respiratory pathogens
including nterobac- teriaceae (K.
pneumoniae, E. coli, Enteroacter spp.), $.
aeruginosa and Sta. aureus especially in
institutionalized subects 23.
Among 5 pathogens isolated Irom
dental plaque and pathogens isolated
Irom OPA specimens, antibiotic
sensitivity patterns showed concordance
oI bacterial cultures between dental
plaque and oropharyngeal cavity isolates
in 13 AP patients. l-Solh et al.
reported that among 33 dental plaque
isolates and 3 OPA isolates,
concordance oI bacterial cultures between
dental plaque and the oropharyngeal
cavity was observed in 0 patients, oI
whom had developed AP 2/.
There were 3 patients who had the same
organism in dental plaque, OPA and
BA specimens. The 3 isolated organisms
(coag- ulase-negative staphylococci, Str.
pneumoniae and K. pneumoniae) displayed
a similar an- timicrobial susceptibility
proIile, suggesting that the etiology oI
AP in such patients could be due to
aspiration oI the organisms Irom dental
plaque or OPA. We also Iound
10 patients with the same organism (Sta. au3
reus) in dental plaque, OPA, BA and blood
specimens. The isolates also had the same an-
timicrobial susceptibility proIile,
suggesting again that AP in such patients
could be due to aspiration oI the organism
Irom OPA or dental plaque or due to
bacteraemia. l-Solh et al. reported in their
study oI critically-ill patients that 1
patients developed AP and oI the 13
isolates recovered Irom BA specimens oI
such patients, showed respi- ratory
pathogens matching those recovered Irom
the corresponding dental plaque by
antibiotic susceptibility testing Sta. aureus
>a<le J C=e and X-reactiFe protein AXR@D leFels in serum and saliFa of patients Iith hospital-acquired pneumonia A]C@D and
controls
@arameter ]C@ patients An = LSD Xontrols An = NSD t-Falue P-Falue
Age (years)
8ean A9:D
50.5 (8.)
8ean A9:D
.8 (.) 1. 0.1
Serum CRP (gm) 8. (1.0) .8 (1.1) 11. 0.001
Saliva CRP (gm) 11. (.) 1. (0.8) 8.3 0.001
S! : standard de'iation.
(5 patients), E. coli (1 patient), E. cloacae
(1 patient) and $. aurginosa (1 patient)
2/.
Quantitative changes oI
speciIic salivary biomarers could
have sig- niIicance in the diagnosis
and manage- ment oI both oral and
systemic diseases 26. n our study
CRP levels in serum and saliva were
signiIicantly higher than those in the
controls. Also there was a signiIicant
correlation between serum and
salivary CRP in patients and in
controls and by linear regression curve.
Christodoulides et al. Iound signiIicant
diIIerences in CRP levels between peri-
odontitis patients with diIIerent grades
oI oral health and normal subects 20.
Salzberoet al. in his study oI 3 patients
with generalized aggressive periodonti-
tis and 1 healthy controls showed that
sera Irom patients with
periodontal inIections contain
elevated levels oI CRP compared
with individuals with good
periodontal health 21.
Xonclusions
nadequate oral hygiene resulting
in Iormation oI dental plaque
bioIilms may promote oral and
oropharyngeal colonization oI
respiratory pathogens
which increase the ris Ior serious lower
respiratory tract inIection
including pneumonia in
hospitalized subects. There is a need
Ior Irequent proIessional oral health
care, education and pro- vision
among high-ris people in the
community and those in intensive care
units.
Cc^noIled=ements
The authors than r Waheed
shac Shenouda, microbiology
laboratory technician, Ior his generous
help in pre- paring the microbiological
media.
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11.
1.
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B<_ectiFes of the `]B Ylo<al Bral ]ealth @ro=ramme
Oral health is part oI total health and essential to quality oI liIe and WO proects intend to translate the evidence into
action programmes. The Oral ealth Programme thereIore gives priority to integration oI oral health with general
health programmes at community or national levels. The WO Oral ealth Programme wors Irom the liIe-course
perspective, currently community programmes Ior improved oral health oI the elderly and oI children is given high
priority.
Further inIormation about the WO lobal Oral ealth Programme can be Iound at h tt p w w w .w h o .i n to ral
healthen