Intensive Care Med (2014) 40:23–31

DOI 10.1007/s00134-013-3049-y ORIGINAL

Eduardo H. Bergan
Bernardo R. Tura
Impact of improvement in preoperative oral
Cristiane C. Lamas health on nosocomial pneumonia in a group
of cardiac surgery patients: a single arm
prospective intervention study

Received: 3 April 2013 Abstract Purpose: To evaluate patients in the preoperative period.
Accepted: 25 July 2013 the effects of an oral health protocol The presence of tongue plaque (OR
Published online: 7 August 2013 on the incidence of postoperative 17, P \ 0.001) and of poor hygiene
Ó Springer-Verlag Berlin Heidelberg and pneumonia in patients submitted to of the total superior dentures (OR 25,
ESICM 2013 P \ 0.001) in the preoperative period
coronary artery bypass grafting and to
valve surgery. Methods: All significantly increased the chance of
patients admitted to a public cardiac PP. The use of CXG 0.12 % in the
surgery hospital were examined by a preoperative period (OR 0.06,
dentist and had a thorough dentistry P \ 0.001) and on the day of surgery
anamnesis and an intraoral exam (OR 0.002, P \ 0.001) was protective
E. H. Bergan
B. R. Tura
C. C. Lamas
Instituto de Pesquisa Evandro Chagas IPEC, focusing on teeth, gums, and tongue.
against PP. Mortality in patients
Fiocruz, Rio de Janeiro, RJ, Brazil Patients were taught how to brush without pneumonia was 9/208
their teeth and tongue and how to (4.32 %) vs. 6/19 (33.3 %) in those
B. R. Tura
clean their jugal and palatal mem- with pneumonia. The presence of
e-mail: brtura@gmail.com
branes. Chlorhexidine gluconate pneumonia increased the chances of
C. C. Lamas (CXG) 0.12 % oral rinse twice a day death by 11 times (P \ 0.001). The
e-mail: cristianelamas@gmail.com mean pneumonia rate in ICU in the
was used until surgery. Data on age,
E. H. Bergan
B. R. Tura
C. C. Lamas sex, comorbidities, oral evaluation, 6 months before the study protocol
Instituto Nacional de Cardiologia INC, type of surgery, and development of was 32 per 1,000 ventilator-days, 24
Rua das Laranjeiras 374, 5° Andar, pneumonia were obtained. Statistical during the 6-month intervention per-
Rio de Janeiro, RJ 22240-006, Brazil analysis was done on these variables iod, and 10 during the next 6 months
to evaluate the impact of the study following the study. Conclu-
C. C. Lamas protocol. Results: A total of 226 sions: PP rates were reduced using
Universidade do Grande Rio, Unigranrio, a simple and efficient protocol of
Rio de Janeiro, RJ, Brazil
patients were enrolled, 136 male
(60.2 %). The median age was dental care that improved oral
E. H. Bergan ()) 59 years. There were 123 (54.4 %) hygiene in the preoperative period of
Rua Capim Branco, No 173 Apartamento patients with coronary artery disease cardiac surgery patients.
303 Vila Valqueire, Rio de Janeiro, and 103 (45.6 %) with valve disease.
RJ 21330-050, Brazil There were 18/226 (8 %) postopera- Keywords Ventilator-associated
e-mail: ehbergan@hotmail.com tive pneumonias (PP), nine in each pneumonia
Chlorhexidine

group. Ten occurred in dentate Cardiac surgical procedure

C. C. Lamas
Avenida Oswaldo Cruz No. 46 apto 501, patients and eight in edentulous ones. Oral hygiene
Tongue
Dentures
Flamengo, Rio de Janeiro, Oral health optimization was
RJ 22250-060, Brazil achieved in 208/226 (92 %) of
24

Introduction Chlorhexidine gluconate (CXG) mouthwash is an

antiplaque agent that is effective at low concentrations
Pneumonia is an infection of the lungs, and bacterial with little, if any, absorption from the gastrointestinal
pneumonia is a common and significant cause of mortality tract and the oral mucous membrane [13]. At the present
and morbidity in human populations [1]. time there is no evidence to support the use of one oral
Ventilator-associated pneumonia (VAP) is defined as a rinse over another in mouth care, the exception being the
nosocomial pneumonia that develops in patients on use of CXG 0.12 % in cardiac surgery patients [11].
mechanical ventilation for 48 h or more, and patients with The mean rate of postoperative pneumonia (PP) in
VAP have high hospital mortality [2]. VAP has high cardiac surgery patients in the Instituto Nacional de
morbidity and mortality in the ICU; mortality ranges from Cardiologia (INC) was 32 per 1,000 ventilator-days in the
24 to 50 %. Two types of VAP are distinguished: early- 6 months before the intervention, well above that reported
onset VAP, diagnosed within the first 96 h of mechanical in the literature (around 14 per 1,000) [14]. A protocol
ventilation, and late-onset, occurring thereafter. The was implemented including oral hygiene instructions,
mechanical process of intubation compromises the natural toothbrushing, tongue and denture hygiene in association
barrier between the oropharynx and trachea and facilitates with the use of CXG 0.12 % oral rinse. The goal was to
the entry of bacteria into the lungs around the endotra- reduce PP rates, particularly in the coronary artery bypass
cheal tube cuff [3]. It is difficult to completely prevent grafting (CABG) group, because no routine dental care
secretions of the oropharynx from invading the airway was offered to them at INC, a procedure that differs from
through the space around the cuff of the tracheal tube, and that adopted for patients with valvular heart disease.
the pooling of secretions around the cuff may provide a
reservoir for pathogenic bacteria [3].
VAP was confirmed as the main cause of postopera-
tive infection in patients undergoing major heart surgery Methods
[4].
Nosocomial pathogens may be part of the host’s Patients were recruited during a 6-month period after their
endogenous flora, or may be acquired from other patients, admission to INC, a federal public hospital located in Rio
staff, devices, or the hospital environment [5]. The oral de Janeiro, Brazil. Patients were invited by the principal
cavity may be an important reservoir of bacteria respon- investigator to participate in the study by signing the
sible for causing lung infection [1]. Oropharynx informed consent form (ICF). Forty-two patients were
colonization is important for the development of respi- excluded, and 226 were included. The study was
ratory infection, because oral microorganisms of critically approved by the institutional review board of this hospital
ill adults differ from those of healthy adults [6]. under number 0307/26.01.2011.
The surface of the tongue facilitates the accumulation Inclusion criteria were being 18 years of age or older;
of nutrient-rich dietary debris. The biofilm on the tongue’s a candidate for heart valve surgery (valve repair or
surface is packed less densely than in periodontal plaque, replacement); a candidate for CABG; and signing the
so this probably facilitates nutrient delivery into saliva. ICF. The exclusion criterion was a history of pneumonia
The killing of bacteria in the biofilm requires antibiotic/ less than 2 weeks prior to admission.
disinfectant concentrations 10–1,000 times those needed Patients were examined in the dentistry unit by the
to kill free-living forms, and the most effective way to same dentist (EHB). Examination consisted of a medical
treat biofilm is by mechanical debridement or removal [7]. and dentistry anamnesis, and an intraoral exam of the oral
Edentulous elderly patients with the presence of tongue and palatal mucosal tissue, tongue, and teeth. During
coating have demonstrated significantly higher salivary examination, some indices were obtained:
bacterial counts than those with no tongue coating [8].
People with teeth or dentures have nonshedding sur- (a) Decayed, missing, and filled teeth index (DMFT),
faces on which biofilms form, and these biofilms are which determines the total number of permanent teeth
susceptible to colonization by respiratory pathogens [9]. that have past or present carious lesions [15].
A systematic review of the literature studying the asso- (b) Simplified oral hygiene index (OHI-S) by (Greene
ciation between poor oral hygiene and the risk of and Vermillion 1964). This quantifies the plaque and
nosocomial pneumonia and chronic lung disease found calculus index and allows classification of oral
that improving oral hygiene can significantly reduce the hygiene [16]. Oral hygiene was classified after the
incidence of pulmonary disease [10]. According to cur- oral hygiene index and was calculated by the totality
rent evidence, it appears that toothbrushing has beneficial of debris index ? calculus index by the following
effects in reducing dental plaque colonization [11] and scores: 0–1, satisfactory; [1.1, unsatisfactory [17].
chlorhexidine may effectively reduce oropharyngeal col- (c) Community periodontal index of treatment needs
onization and VAP [12]. (CPITN), which was used to determine the periodontal
 25

needs, and to quantify periodontal disease: (0) healthy the bed (HOB) (30–45°); daily ‘‘sedation vacations’’ and
periodontal tissues; (1) bleeding after gentle probing; assessment of the readiness to extubate; peptic ulcer
(2) supragingival or subgingival calculus or defective disease prophylaxis (all patients were administered ant-
margin of filling or crown; (3) 4 or 5 mm pocket; (4) acids, ranitidine or omeprazole, as a postoperative
6 mm or deeper pathologic pocket [18]. Patients were protocol for gastric bleeding prevention in cardiac sur-
considered as having periodontal disease if they gery); and deep venous thrombosis/pulmonary
received the score number 4. thromboembolism (DVT/PE) prophylaxis for all ICU
(d) The additive index, which quantifies the plaque of patients requiring mechanical ventilation. Pneumonia
total maxillary dentures, with a score between 0 and rates were expressed by the number of pneumonias per
15 points was recorded in five defined areas on the 1,000 days of mechanical ventilation, as per the Centers
denture base: 0, no visible plaque; 1, plaque visible for Disease Control and Prevention National Healthcare
only by scraping on the denture base; 2, moderate Safety Network (CDC/NHSN) definition [22]. All pro-
accumulation; 3, abundant plaque [19]. All dentures cedures were registered and collected in a specific record
with a score greater than 10 were considered to be in sheet. A control group was considered unethical by the
a state of poor hygiene. ethics committee.
Totally edentulous patients were assessed in terms of
the hygiene of the total maxillary dentures and of the Statistical analysis
tongue.
The presence of active infectious foci such as teeth or Percentages were calculated for discrete variables, and
residual roots with active carious lesions, residual roots median and interquartile ranges for continuous variables.
with endodontic material exposed in the intraoral envi- The association between categorical variables was made
ronment, inflamed gums with suppuration, teeth mobility by contingency tables analyzing Pearson chi-squared test
with subgingival calculus and oral candidiasis was eval- or Fisher’s exact test. All continuous variables did not
uated in all patients. show Gaussian distribution in the Shapiro–Wilk test and
Patients were instructed on how to brush their teeth by therefore a non-parametric test was used. The Mann–
using the Bass technique [20], cleaning the palate, the Whitney non-parametric test was used to verify differ-
tongue, and the denture by brushing. They were instructed ences between continuous variables by surgery groups
to use CXG 0.12 % twice a day, after breakfast and before and pneumonia. P values were considered statistically
sleep, by rinsing the mouth with 15 ml for 2 min significant if less than 0.05; any P value less than 0.001
including gargling. They were also instructed to do the was recorded as P \ 0.001. Data were collected and
same process with CXG 0.12 % just before going to the analyzed in the Epi Info statistical program, version 3.3.2
operating room. In the immediate postoperative period (in and Statistical Package for Social Sciences version 16.0.
ICU) nursing staff and/or the responsible dentist (EHB)
performed the oral hygiene protocol twice a day using
toothbrushing and CXG 0.12 % even in intubated
patients. Patients were also instructed to continue the Results
same preoperative protocol as soon as they returned to the
ward. Patients continued to be assessed in the postoper- A total of 226 patients were included, of which 136 were
ative period to observe the effectiveness of oral care and male (60.2 %). The median age was 59 years. There were
were considered to have optimized oral hygiene if they 50.9 % white, 21.7 % black, and 27.4 % mulatto. The
presented with less intraoral plaque and/or if they were median body mass index was 26.8. There were 123
using CXG 0.12 % as recommended. Postoperative (54.4 %) patients with coronary artery disease and 103
pneumonia was diagnosed by the Clinical Pulmonary (45.6 %) with valvular disease. The number of patients
Infection Score (CPIS) modified by Flanagan et al. [21]. submitted to combined surgery (CABG and VS) was 22
Clinical suspicion of VAP was diagnosed from chest (9.7 %), and they were reclassified into VS or CABG
X-rays showing a new, persistent ([24 h), and/or pro- groups according to the main underlying condition. So 16
gressive infiltrate, abscess, cavitation, or suspected (7.1 %) were enrolled in the VS group and 6 (2.6 %) in
empyema, and an increase in the volume and purulence of the CABG group. Forty-two patients were excluded
suctioned secretions, and one or more of the following: because their cardiologist recommended clinical treat-
fever of at least 38 °C for more than 4 h; blood leuko- ment and discharged them.
cytosis of least 11 9 109/l; and an increase in the fraction Patients from the VS group had received 2 g of
of inspired oxygen (FIO2) of 0.2 needed to maintain amoxicillin 1 h before the invasive dentistry treatment as
arterial oxygen saturation, sustained for more than 4 h. endocarditis prophylaxis. Two patients from the VS group
A CPIS of at least 6 was very suggestive of pneumonia were treated for endocarditis with vancomycin, and four
[21]. The VAP bundle included elevation of the head of patients from the CABG group were treated with
26

clindamycin for an odontogenic infection before surgery. After oral health optimization, on evaluation just
All patients received 2 g of cefazolin 30 min before before surgery, the two surgery groups were no longer
cardiac surgery as wound infection prophylaxis except statistically different, P = 0.74.
those treated for endocarditis, who received extended The oral health classification just before surgery of all
prophylaxis with vancomycin and ciprofloxacin for 24 h. 18 patients who had PP was satisfactory in 1 (5.6 %),
The two surgical groups were compared before cardiac unsatisfactory in 9 (50.0 %), and 8 patients (44.4 %) were
surgery. Comorbidities, sociodemographic characteristics, edentulous.
and oral hygiene status are shown in Table 1 and con- There were 18/226 (8 %) postoperative pneumonias,
tinuous variables are shown in Table 2. nine in each group. Ten occurred in dentate patients and 8
The oral health classification in the VS group in the in edentulous ones. There were 7 (38.9 %) women and 11
first dentistry evaluation was satisfactory in 49.5 %, (61.1 %) men. The median time of ICU stay was greater
unsatisfactory in 27.5, and 23.0 % of patients were totally in patients who developed pneumonia (17.5 days) than
edentulous. those that did not (5.0 days), P \ 0.001.
The oral health classification in the CABG group Comorbidities, sociodemographic characteristics, and
in the first dentistry evaluation was satisfactory in 27.6 %, oral hygiene status in patients with and without PP are
unsatisfactory in 35.8, and 36.6 % were totally shown in Table 3 and continuous variables are shown in
edentulous. Table 4. Although male sex, diabetes, and tobacco use
The first dentistry evaluation showed that the two were more prevalent in the CABG group, only hyper-
surgery groups were different, with the VS group having tension was shown to increase the chance of pneumonia,
2.3 times more chance of having satisfactory hygiene, and hypertension may be a confounding variable. Patients
P = 0.01. with unsatisfactory oral hygiene had 12 times the chance
Oral health optimization was achieved in 208/226 of developing PP compared with the ones with satisfac-
(92 %) of patients in the preoperative period, 93.5 % in tory oral hygiene (P = 0.004).
the CABG group and 90.5 % in the VS group. A total of The presence of tongue plaque (OR 17, P \ 0.001)
60.2 % patients from the CABG group were classified as and of poor hygiene of the total superior dentures (OR 25,
having satisfactory oral hygiene just before surgery P \ 0.001) in the preoperative period significantly
compared to 27.6 % in the first evaluation, whereas increased the chance of PP.
70.9 % of patients from the VS group had satisfactory The use of CXG 0.12 % in the preoperative period
oral hygiene just before surgery compared to 49.5 % in (OR 0.06 P \ 0.001) and on the day of surgery (OR 0.002
the first evaluation. P \ 0.001) was protective against PP.

Table 1 Distribution of variables for gender, comorbidities, past (candidates for valve surgery and coronary artery bypass grafting
history of pneumonia, oral hygiene classification before surgery, surgery), INC 2011
and optimization of oral hygiene in the 226 cardiac surgery patients
Variables Surgery groups Odds ratio [95 % CI] P value
VS CABG
N (%) N (%)

Gender
Female 60 (58.3) 30 (24.4) 0.2 [0.10–0.40] \0.001a
Male 43 (41.7) 93 (75.6) 1.00
Debris on tongue 50 (41.3) 71 (58.7) 0.7 [0.40–1.20] 0.2
Active oral infection 21 (32.8) 43 (67.2) 0.5 [0.26–0.88] 0.02a
Periodontal disease (CPITN) 3 (16.7) 15 (83.3) 0.2 [0.06–0.76] 0.02a
Totally edentate 24 (34.7) 45 (65.2) 0.5 [0.30–0.94] 0.04a
Debris on denture (additive index) 25 (34.2) 48 (65.8) 0.5 [0.30–1.16] 0.1
Calculus on denture (additive index) 7 (36.9) 12 (63.1) 0.8 [0.30–2.30] 0.9
TSD with poor hygiene (additive index) 9 (30.0) 21 (70.0) 0.5 [0.20–1.20] 0.2
OHO by dentistry treatment 75 (72.8) 20 (16.3) 0.1 [0.03–0.13] \0.001a
OHO by improvement of oral hygiene 93 (90.3) 115 (93.5) 1.5 [0.60–4.00] 0.52
Diabetes 8 (7.8) 42 (34.1) 0.1 [0.07–0.36] \0.001a
Tobacco use 45 (43.7) 79 (64.2) 0.4 [0.25–0.75] 0.003a
Past medical history of pneumonia 33 (32.0) 20 (16.3) 2.4 [1.30–4.50] 0.007a
VS valve surgery, CABG coronary artery bypass grafting, CI confidence interval, CPITN community periodontal index of treatment needs,
TSD total superior denture, OHO oral health optimization
a
Chi-squared test, significant
 27

Table 2 Distribution of continuous variables before surgery in the 226 cardiac surgery patients (candidates for valve surgery and
coronary artery bypass grafting surgery), INC 2011

Variables Surgery groups P valuea

VS CABG
Median [IQR] Median [IQR]

Age (years) 53 [41–64] 63 [56–68] \0.001b

Body mass index 26.7 [22.6–30.3] 27.1 [24.4–30.1] 0.20
Monthly Income (1 unit = US$311) 2 [1–3] 3 [2–5] \0.001b
TSD biofilm score (additive index) 6 [5–10] 7 [4–12] 0.4
DMFT index 22 [12–32] 24 [17–32] 0.03b
Decayed (D) 0 [0–0] 0 [0–1] 0.23
Missing (M) 13 [6–29] 22 [10–32] 0.003b
Filled (F) 1 [0–7] 0 [0–4] 0.005b
Time between intervention and surgery (days) 12 [8–18] 5 [2–11] \0.001b
Days of mechanical ventilation 1 [1–2] 1 [1–2] 0.22
VS valve surgery, CABG coronary artery bypass grafting, IQR interquartile range (25–75 %), TSD total superior denture, DMFT
(decayed, missing, filled teeth)
a
Mann–Whitney test
b
Significant p \ 0.05

Table 3 Distribution of variables for comorbidities, sociodemo- valve surgery and coronary artery bypass grafting surgery) with and
graphic characteristics, oral hygiene classification, and optimization without postoperative pneumonia, INC 2011
of oral hygiene in the 226 cardiac surgery patients (candidates for
Variables Pneumonia Odds ratio [95 % CI] P value
Yes No
N (%) N (%)

Gender
Female 7 (38.9) 83 (39.9) 1.04 [0.38–2.80] 0.90
Male 11 (61.1) 125 (60.1) 1.00
Debris on tongue 17 (94.4) 104 (50.0) 0.06 [0.008–0.45] \0.001a
Active oral infection 5 (27.8) 59 (28.4) 0.97 [0.33–2.84] 0.95
Periodontal disease (CPITN) 3 (16.7) 15 (7.2) 0.38 [0.10–1.50] 0.16b
Totally edentate 8 (44.4) 61 (29.3) 0.51[0.20–1.37] 0.28
Debris on denture (additive index) 9 (50.0) 64 (55.7) 0.14 [0.01–1.11] 0.04b
Calculus on denture (additive index) 7 (77.8) 12 (10.4) 0.03 [0.006–0.18] \0.001b
TSD with poor hygiene (additive index) 8 (88.9) 22 (24.2) 0.04 [0.005–0.34] \0.001b
OHO by dentistry treatment 5 (27.8) 90 (43.3) 0.50 [0.17–1.46] 0.30
OHO by improvement of oral hygiene 4 (22.2) 204 (98.1) 0.0056 [0.001–0.02] \0.001b
Surgery groups CABG 9 (50.0) 114 (54.4) 1.22 [0.46–3.18] 0.90
VS 9 (50.0) 94 (45.6) 1.00
Diabetes 6 (33.3) 44 (21.2) 1.86 [0.66–5.25] 0.18b
Tobacco use 8 (44.4) 116 (55.8) 1.24 [0.46–3.34] 0.84a
Past medical history of pneumonia 4 (22.2) 49 (23.6) 0.98 [0.30–3.20] 1.0b
CI confidence interval, CPITN community periodontal index of treatment needs, TSD total superior denture, OHO oral health optimi-
zation, VS valve surgery, CABG coronary artery bypass grafting
a
Chi-squared test, significant
b
Fisher’s exact test, P \ 0.05

In the preoperative period, 107 (87 %) patients in the The mean VAP rate in the 6 months previous to the
CABG group and 94 (91.3 %) in the VS group used CXG study protocol was 32 per 1,000 ventilator-days and it
0.12 %. On the day of surgery, 109 (88.6 %) patients in was 24 per 1,000 ventilator-days during the 6-month
the CABG group and 92 (89.3 %) in the VS group used intervention period. During the next 6 months
CXG 0.12 %. following the study, with continuity of implemented
The presence of pneumonia increased the chances of measures by ICU staff, the rate was 10 per
death by 11 times, P \ 0.001. Mortality in patients 1,000 ventilator-days.
without pneumonia was 9/208 (4.32 %) vs. 6/19 (33.3 %) Microbiological features of the 18 patients who
in those with pneumonia. developed PP are shown in Table 5.
28

Table 4 Distribution of continuous variables in the 226 cardiac surgery patients (candidates for valve surgery and coronary artery bypass
grafting surgery) with and without postoperative pneumonia, INC 2011

Variables Pneumonia P valuea

Yes No
Median [IQR] Median [IQR]

Age (years) 60.5 [55–73] 59.0 [50–67] 0.2

Body mass index 26.85 [25.7–27.8] 26.85 [23.7–30.2] 0.6
Monthly income (1 unit = US$311) 1.75 [0–3] 2.5 [1.5–4] 0.04b
TSD biofilm score (additive index) 13 [13–13] 6.0 [4–10] \0.001b
DMFT index 30 [21–32] 22 [14.5–32] 0.03b
Decayed (D) 0 [0–0] 0 [0–1] 0.95
Missing (M) 26 [16–32] 17 [8–32] 0.07
Filled (F) 0 [0–4] 0 [0–6] 0.34
Time between intervention and surgery (days) 10.5 [8–15] 9.0 [4–14.5] 0.3
Days of mechanical ventilation 11 [4–18] 1 [1–2] \0.001b
IQR interquartile range (25–75 %), TSD total superior denture, DMFT (decayed, missing, filled teeth)
a
Mann–Whitney test
b
Significant, P \ 0.05

Table 5 Microbiological documentation, CPIS score, pneumonia classification, and outcome of 18 patients with postoperative pneu-
monia, INC 2011

Patient number Microbiology (isolated organisms) CPIS score Pneumonia classification Death
a c
1 Acinetobacter baumannii 10 Early-onset VAP Yes
2 Gram negative rod (not identified) 8 Late onset VAPd No
3 Escherichia coli 6 Early-onset VAP Yes
4 Enterobacter aerogenes 4 Hospital-acquired pneumonia (not VAP) No
5 Enterobacter cloacae 5 Late onset VAP Yes
6 E. cloacae 7 Late onset VAP Yes
7 E. cloacae 7 Late onset VAP No
8 Klebsiella oxytoca 6 Hospital-acquired pneumonia (not VAP) No
9 K. pneumoniae 8 Late onset VAP Yes
10 Not identifiedb 9 Hospital-acquired pneumonia (not VAP) Yes
11 Not identifiedb 8 Late onset VAP No
12 Serratia marcescens 5 Late onset VAP No
13 S. marcescens 8 Late onset VAP No
14 S. marcescens and A.baumannii 7 Late onset VAP No
15 S. marcescens and Proteus mirabilis 7 Late onset VAP No
16 MRSA 5 Late onset VAP No
17 Not identified 6 Early-onset VAP No
18 Not identified 8 Late onset VAP No
MRSA methicilin-resistant Staphylococcus aureus d
Late onset: pneumonia that occurred after 96 h of mechanical
a
Multiresistant ventilation
b
No respiratory specimens were sent
c
Early onset: pneumonia that occurred within less than 96 h of
mechanical ventilation

A subgroup analysis was done for the patients who Discussion

were ventilated for more than 2 days, comparing the 15
patients who had pneumonia to the 17 that did not have In this study, the characteristics of oral hygiene and
pneumonia. Oral hygiene optimization occurred more postoperative pneumonias were compared between two
often in the no-pneumonia group (OR 64, P \ 0.001), as cardiac surgery groups, VS and CABG. Patients with
well as the use of chlorhexidine preoperatively (OR 104, valve disease, historically, in our institute, showed lower
P \ 0.001) and on the day of surgery (OR 136, rates of PP probably owing to better oral hygiene. Patients
P \ 0.001). Poor denture hygiene was more frequent in in this group have increased risk of endocarditis [23] and
those with pneumonia (OR 31.5, by Fisher’s, P = 0.005). are frequently referred by physicians for dental care. After
There were no differences between the two subgroups in the protocol was implemented for all patients, there was a
age, gender, or mortality. reduction in the overall rate of PP, and no difference was
 29

seen between the VS and CABG groups, meaning that the Oral care with the use of CXG is part of the European
protocol worked well for both groups. care bundle for prevention of VAP [32], and oral care was
A large amount of dental plaque brings a high risk for recognized by the CDC as a modifiable risk factor for
development of VAP [24] and therefore risk reduction for preventing VAP [33]. We have included oral hygiene in
PP was the goal of this oral intervention study [25]. the pneumonia bundle at our hospital following the results
Biofilm adheres and colonizes mucosal surfaces, of this intervention.
teeth, dorsum of the tongue, and foreign bodies including It seems that oral disinfection with CXG [34] and
dentures and the endotracheal tube [12]. In edentulous mechanical oral hygiene with toothbrushing are required
people, dentures may easily serve as a reservoir for for optimal oral health [35]. A systematic review on
bacteria if they are not properly cleaned. The surgery toothbrushing in VAP found a significant reduction in
groups were not different in the preoperative period for rates in the trial at low risk of bias, and when all trials
debris on the tongue, debris on the denture, calculus on were considered, there was a trend toward lower VAP
the denture, and total superior denture with poor rates [35]. In accordance with a meta-analysis and the
hygiene; however, the groups were different concerning American Association of Critical Care Nursing, CXG and
periodontal disease. Scannapieco and Genco [10] showed mechanical oral care need further studies so that their
the potential correlation of periodontal disease with effects can be clearly explained and elucidated [36, 37].
VAP, but in our study the correlation of periodontal Although the importance of toothbrushing in reducing
disease with PP was not significant, possibly because 14 VAP rates is recognized [35], the role of brushing oral
of the 18 patients diagnosed in the preoperative period surfaces needs further evaluation. We need more research
with periodontal disease had their oral hygiene improved on this aspect of oral care to evaluate its potential,
by the protocol measures. The CABG group showed a because until now no effect on reducing VAP, mortality,
higher percentage of active oral infection, compared with or length of stay has been proved, especially in cardiac
the VS group, but the number of patients who went to surgery patients. We believe CXG alone can make
surgery with active oral infection was small, as they intraoral plaque less pathogenic, but removing the intra-
were treated before surgery. oral plaque can reduce bacterial lung translocation. It was
In two studies, the authors excluded edentulous not the purpose of this study to compare CXG alone and
patients [26, 27]. In our study, this could not be done as CXG associated with toothbrushing, because the goal was
there were a large number of edentulous people (30.5 %), to offer optimal health care for all patients with a com-
and pneumonia was significantly linked with the presence bined mechanical and chemical approach.
of tongue plaque and poor hygiene of the total superior As shown in other studies, PP is related to longer
denture (variables not linked with teeth). Before this ventilator times following surgery and higher mortality
study, edentulous patients were not sent for dental eval- rates. Other variables, such as depth of sedation, may
uation in INC prior to cardiac surgery. This practice has account for this, and although daily awakening from
changed, and all patients, dentate or not, are now exam- sedation is part of the VAP protocol implemented in our
ined in the preoperative period. ICU, it was not systematically studied in this report [38].
Although oral rinse with CXG is generally accepted as Patients ventilated for more than 2 days in this study still
an effective measure to reduce the risk of VAP, including experienced a protective effect with the use of chlorhex-
in cardiac surgery patients [28], it remains unclear which idine preoperatively and with oral health optimization,
concentration to use, what the exposure time should be, and pneumonia was associated with poor denture hygiene.
and how frequently it should be performed [14]. A study Therefore, despite the possibility of cardiac, respiratory,
in a surgical/trauma/burn ICU, using toothbrushing for and neurological failure in those with more than 2 days of
1–2 min twice a day with 15 ml of CXG 0.12 % solution ventilation, the protocol protected even these more vul-
achieved a 46 % reduction in VAP rates [29]. Using the nerable patients from pneumonia.
same protocol in the preoperative period, we achieved a During the study period, endotracheal tubes with
25 % reduction in 6 months and 69 % in 12 months, subglottic drainage were not used; therefore, this con-
showing that this protocol was effective in the setting of founding variable was absent [14]. This form of
patients submitted to cardiac surgery in a developing prevention is valid and has been shown in another Bra-
country. zilian hospital [34]; however, avoiding secretions that
Recent surveillance data in which 173 ICUs from reach the area around the cuff is the critical issue, and we
different continents were involved, the estimated pooled have focused on oral hygiene and CXG 0.12 % use. Since
mean of VAP was 13.6 per 1,000 ventilator-days [14]. In microaspiration of secretions is an etiological factor for
our study, similarly to that by Garcia et al. [30], VAP VAP, oral suctioning and practices for management of the
rates decreased during and after the intervention period. cuffs of endotracheal tubes (pressure over 20 cmH2O) are
We observed in the study that 92 % of patients improved very important [39]. The costs of endotracheal tubes with
oral hygiene, and systematic oral care can improve oral a subglottic device may be too high for routine use in our
health in critically ill patients [31]. scenario and need to be further evaluated [40].
30

Limitations showing the importance of improving oral hygiene in the

preoperative and postoperative period of patients sub-
Firstly, although CXG 0.12 % showed very good results, mitted to cardiac surgery.
the study was not controlled for that. Secondly, this is a
single center study in the setting of a developing country Acknowledgments We would like to thank all medical personnel
and results may not be amenable to extrapolation. in the ICU and all colleagues from the Dentistry Department; and
Dr. Armando de Oliveira Schubach, Dr. Raquel de Vasconcellos C.
de Oliveira and Dr Claudia Maria Valete Rosalino from IPEC,
Fiocruz, for reviewing the paper critically; and José Emanuel Félix,
from the Infection Control Unit (INC), for logistics support.
Conclusions
Conflicts of interest On behalf of all authors, the corresponding
author states that there is no conflict of interest.
PP rates were reduced during the study period and the
incidence of PP in CABG and VS groups decreased,

References
1. Paju S, Scannapieco FA (2007) Oral 11. Berry AM, Davidson PM, Nicholson L 21. Flanagan PG, Findlay GP, Magee JT
biofilms, periodontitis, and pulmonary et al (2011) Consensus based clinical et al (2000) The diagnosis of ventilator-
infections. Oral Dis 13:508–512 guideline for oral hygiene in the associated pneumonia using non-
2. Hutchins K, Karrus G, Erwin J et al critically ill. Intensive Crit Care Nurs bronchoscopic, non-directed lung
(2009) Ventilator-associated 27:180–185 lavages. Intensive Care Med 26:20–30
pneumonia and oral care: a successful 12. Halm MA, Armola R (2009) Effect of 22. Horan TC, Andrus M, Dudeck MA
quality improvement project. Am J oral care on bacterial colonization and (2008) CDC/NHSN surveillance
Infect Control 37(7):590–597 ventilator-associated pneumonia. Am J definition of healthcare-associated
3. American Thoracic Society, Infectious Crit Care 18:275–278 infection and criteria for specific types
Diseases Society of America (2005) 13. Dodd MJ, Dibble SL, Miaskowski C of infections in the acute care setting.
Guidelines for the management of et al (2000) Randomized clinical trial of Am J Infect Control 36:309–332
adults with hospital-acquired, the effectiveness of 3 commonly used 23. Wilson W, Taubert KA, Gewitz M et al
ventilator-associated, and healthcare- mouthwashes to treat chemotherapy- (2007) Prevention of infective
associated pneumonia. Am J Respir Crit induced mucositis. Oral Surg Oral Med endocarditis. Guidelines from the
Care Med 171:388–416. doi: Oral Pathol Oral Radiol Endod American Heart Association. A
10.1164/rccm.200405-644ST 90(1):39–47 guideline from the American Heart
4. Hortal J, Muñoz p, Cuerpo G et al 14. Blot S, Rello J, Vogelaers D (2011) Association Rheumatic Fever,
(2009) Ventilator-associated What is new in the prevention of Endocarditis, and Kawasaki Disease
pneumonia in patients undergoing ventilator-associated pneumonia? Curr Committee, Council on Cardiovascular
major heart surgery: an incidence study Opin Pulm Med 17:155–159 Disease in the Young, and the Council
in Europe. Crit Care 13(3):R80 15. DMFT index. http://classof on Clinical Cardiology, Council on
5. Craven DE (2000) Epidemiology of 2011indexwikisite.wikispaces.com/ Cardiovascular Surgery and Anesthesia,
ventilator-associated pneumonia. Chest DMFT?Index. Accessed May 2013 and the Quality of Care and Outcomes
117:1865–1875 16. Greene JC, Vermillion JR (1964) Research Interdisciplinary Working
6. Garcia R (2005) A review of the Simplified oral hygiene index. Group. Circulation 116:1736–1754
possible role of oral and dental http://www.mah.se/CAPP/Methods- 24. Munro CL, Grap MJ, Elswick RK Jr
colonization on the occurrence of health and-Indices/Oral-Hygiene-Indices/ et al (2006) Oral health status and
care-associated pneumonia: Simplified-Oral-Hygiene-Index-OHI-S/. development of ventilator-associated
underappreciated risk and a call for Accessed May 2013 pneumonia: a descriptive study. Am J
interventions. Am J Infect Control 17. Dos Santos PAT, Fortes TMV, Cabral Crit Care 15:453–460
33:527–541 MCB et al (2008) Influence of sexual 25. Jones DJ, Munro CL, Grap MJ (2011)
7. Drinka PJ, El-Solh AA (2010) The hormones on periodontal tissues in Natural history of dental plaque
tongue, oral hygiene, and prevention of hormonal contraceptives users. Revista accumulation in mechanically
pneumonia in the institutionalized de Periodontia 18(03):55–63 ventilated adults: a descriptive
elderly. JAMDA 11(7):465–467 18. CPITN index. http://classof2011 correlational study. Intensive Crit Care
8. Abe S, Ishihara K, Adachi M et al indexwikisite.wikispaces.com/ Nurs 27(6):299–304
(2008) Tongue-coating as risk indicator CPITN?Index . Accessed May 2013 26. Munro CL, Grap MJ, jones DJ et al
for aspiration pneumonia in edentate 19. Ambjornsen E, Vulderhaug J, Norheim (2009) Chlorhexidine, toothbrushing,
elderly. Arch Gerontol Geriatr PW et al (1982) Assessment of an and preventing ventilator-associated
47:267–275 additive index for plaque accumulation pneumonia in critically ill adults. Am J
9. Scannapieco FA (2006) Pneumonia in on complete maxillary dentures. Acta Crit Care 18(5):428–438
nonambulatory patients. JADA Odontol Scand 40(4):203–208 27. Grap MJ, Munro CL, Hamilton VA et al
137:215–219 20. Bass method. http://www.oralcareshop. (2011) Early, single chlorhexidine
10. Scannapieco FA, Genco RJ (1999) com/bass-method.htm. Accessed May application reduces ventilator-
Association of periodontal infections 2013 associated pneumonia in trauma
with atherosclerotic and pulmonary patients. Heart Lung 40(5):e115–e122
diseases. J Periodontal Res 34:340–345
 31

28. Chlebicki MP, Safdar N (2007) Topical 33. Tablan OC, Anderson IJ, Besser R et al 37. Balamurugan E, Kanimozhi A, Kumeri
chlorhexidine for prevention of (2004) Guidelines for preventing G (2012) Effectiveness of chlorhexidine
ventilator-associated pneumonia: a health-care-associated pneumonia, oral decontamination in reducing the
meta-analysis. Crit Care Med 2003: recommendations of CDC and incidence of ventilator associated
35:595–602 the Healthcare Infection Control pneumonia: a meta-analysis. BJMP
29. Sona CS, Zack JE, Schallom ME et al Practices Advisory Committee. 5(1):a512
(2009) The impact of a simple, low-cost MMWR Recomm Rep 53:1–36 38. Shehabi Y et al (2013) Sedation depth
oral care protocol on ventilator- 34. Caserta RA et al (2012) A program for and long-term mortality in
associated pneumonia rates in a surgical sustained improvement in preventing mechanically ventilated critically ill
intensive care unit. J Intensive Car Med ventilator associated pneumonia in an adults: a prospective longitudinal
37(7):590–597 intensive care setting. BMC Infect Dis multicentre cohort study. Intensive Care
30. Garcia R, Jendresky L, Colbert L et al 12:234 Med 39:910–918
(2009) Reducing ventilator-associated 35. Alhazzani W et al (2013) 39. Sole ML, Byers JF, Ludy JE et al
pneumonia through advanced oral- Toothbrushing for critically ill (2002) Suctioning techniques and
dental care: a 48-month study. Am J mechanically ventilated patients: a airway management practices: pilot
Crit Care 18(6):523–534 systematic review and meta-analysis of study and instrument evaluation. Am J
31. Fourrier F, Duvivier B, Boutigny H et al randomized trials evaluating ventilator- Crit Care 11:363–368
(1998) Colonization of dental plaque: a associated pneumonia. Crit Care Med 40. Muscerede J et al (2011) Subglottic
source of nosocomial infections in 41:646–655 secretion drainage for the prevention of
intensive care unit patients. Crit Care 36. Martin B (2010) Oral care for patients ventilator-associated pneumonia: a
Med 26(2):301–308 at risk for ventilator-associated systematic review and meta-analysis.
32. Rello J, Lode h, Cornaglia G et al pneumonia. http://www.aacn. Crit Care Med 39(8):1985–1991
(2010) A European care bundle for org/wd/practice/content/oral-care-
prevention of ventilator-associated practice-alert.pcms?menu=practice.
pneumonia. Intensive Care Med Accessed May 2013
36:773–780