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Oral Care Interventions and Oropharyngeal Colonization in Children

Receiving Mechanical Ventilation

Article  in  American Journal of Critical Care · August 2009

DOI: 10.4037/ajcc2009121 · Source: PubMed

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Pediatric Critical Care

O RAL CARE INTERVENTIONS

AND OROPHARYNGEAL
COLONIZATION IN
CHILDREN RECEIVING
MECHANICAL VENTILATION
By Mavilde L.G. Pedreira, RN, PhD, Denise M. Kusahara, RN, MNSc, Werther
Brunow de Carvalho, MD, PhD, Silvia Cristina Núñez, DDS, PhD, and Maria
Angélica S. Peterlini, RN, PhD

Background Recent progress in identification of oral microor-

ganisms has shown that the oropharynx can be a site of origin
for dissemination of pathogenic organisms to distant body
sites, such as the lungs.
Objective To compare the oropharyngeal microbiological pro-
file, duration of mechanical ventilation, and length of stay in
the intensive care unit of children receiving mechanical ventila-

C E 1.5 Hours
Notice to CE enrollees:
A closed-book, multiple-choice examination
following this article tests your understanding of
the following objectives:
1. Describe the incidence of ventilator-associated
pneumonia in the pediatric intensive care unit
(PICU) patient population.
2. Identify microorganisms that commonly col-
onize the oropharynx of PICU patients.
3. Recognize the impact of an oral care routine
using chlorhexidine on a PICU study group.
To read this article and take the CE test online,
visit www.ajcconline.org and click “CE Articles
in This Issue.” No CE test fee for AACN members.
©2009 American Association of Critical-Care Nurses
doi: 10.4037/ajcc2009121
tion who had pharmacological or nonpharmacological oral care.
Methods A randomized and controlled study was performed
in a pediatric intensive unit in São Paulo, Brazil. A total of 56
children were randomly assigned to an experimental group
(n = 27, 48%) that received oral care with use of 0.12% chlorhexi-
dine digluconate or a control group (n = 29, 52%) that received
oral care without an antiseptic. Oropharyngeal secretions were
collected and cultured on days 0, 2, and 4, and at discharge.
Results The 2 groups had similar demographic characteris-
tics, preexisting underlying diseases, and pharmacological,
nutritional, and ventilatory support. Gram-negative bacteria
were the predominant pathogens: Acinetobacter baumannii,
Pseudomonas aeruginosa, Klebsiella pneumoniae, and Enter-
obacter species. The 2 groups did not differ significantly in the
colonization of normal (P = .72) or pathogenic (P = .62) flora, in
the duration of mechanical ventilation (P = .67), or in length of
stay in the intensive care (P = .22).
Conclusion Use of chlorhexidine combined with nonpharma-
cological oral care did not decrease the colonization profile,
duration of mechanical ventilation, or length of stay in critically
ill children receiving mechanical ventilation. (American Journal
of Critical Care. 2009;18:319-329)

www.ajcconline.org AJCC AMERICAN JOURNAL OF CRITICAL CARE, July 2009, Volume 18, No. 4 319
 V
entilator-associated pneumonia (VAP) is among the most frequently occurring
nosocomial infections in critical care patients.1-5 A rate of 11.6 VAP episodes per
1000 days of mechanical ventilation in a pediatric intensive care unit (PICU) in
the United States has been reported.6 In studies in Mexico7 and Brazil,8 rates were
28 and 18.7 episodes, respectively, per 1000 days of mechanical ventilation. Results
from the US National Nosocomial Infections Surveillance System indicate that pneumonia
accounts for approximately 15% of all hospital-associated infections, ranging from 4.7 cases
in PICUs to 34.4 cases in burn ICUs.9 VAP accounts for 18% of the nosocomial infections in
infants less than 2 months old, 20% of those in children between 2 months and 5 years old,
26% in children between 5 and 12 years old, and 21% in children more than 12 years old.6

Patients receiving mechanical ventilation have
decreased salivary secretion, and oral cavity hygiene
worsens, resulting in bacteria overgrowth.10 Oropha-
ryngeal colonization with potentially pathogenic
microorganisms is crucial in the pathogenesis of VAP.
Oral care regimens that improve oral health status
and modulate bacterial overgrowth could reduce
the development of nosocomial VAP.1-4,11-15
Grap et al16 investigated the relationship between
VAP and oral health status in a sample of 34 adults
receiving mechanical ventilation. Alterations in oral
health status occurred during the first
7 days after intubation, with micro-
Pneumonias bial colonization of the oropharynx
account for 15% and trachea. Dental plaque and oral
organisms increased over time; poten-
of all hospital- tial pathogens were identified in cul-
tures of oral samples before or at the
associated same time as the appearance of these
infections. organisms in tracheal aspirates, and
higher dental plaque scores correlated
with an increased risk for VAP.
The Centers for Disease Control and Prevention
guidelines9 for preventing health care–associated
pneumonia recommend the development and imple-
mentation of a comprehensive oral hygiene program
About the Authors
Mavilde L.G. Pedreira and Maria Angélica S. Peterlini are
adjunct professors and Denise M. Kusahara is a pediatric
critical care nurse, Nursing School, and Werther Brunow
de Carvalho is an adjunct professor, Pediatrics Department,
of the Federal University of São Paulo, Brazil. Silvia
Cristina Núñez is a professor, Research Center for Den-
tistry Training and Advancement, São Paulo, Brazil.
Corresponding author: Mavilde Luz Gonçalves Pedreira,
Nursing School, Federal University of São Paulo, Rua
Napoleão de Barros, 754 office 113, Vila Clementino-São
Paulo-Capital, Brazil CEP 04024002 (e-mail: mpedreira
@unifesp.br).
for patients in acute care settings who are at high
risk for this type of pneumonia. Essentially 2 tech-
niques are described to remove dental plaque and
associated microbes in critically ill patients: mechan-
ical intervention and direct pharmacological interven-
tion with antimicrobial agents.17 Although mechanical
removal may be an effective method for eliminating
oral pathogens, and oral hygiene is considered stan-
dard nursing care, oral care is often neglected in
critically ill patients or is performed by quickly
swabbing the patient’s mouth.18
In a study19 to determine the frequency of oral
care performed by nurses, the majority of nurses
reported that they provided oral care 5 or more
times per day for any patient who was intubated,
but oral care was documented only a mean of 1.2
times per patient. Toothbrushing was used signifi-
cantly more often in nonintubated patients than in
intubated patients (P < .001), whereas sponge too-
thette swabs were used significantly more often in
intubated patients than in nonintubated patients (P <
.001). Similarly, Hanneman and Gusick20 high-
lighted that the use of mouthwash, toothbrush, and
toothpaste, as well as the frequency of oral care
interventions, was lower in intubated patients than
in nonintubated patients.
DeRiso et al21 showed that inexpensive and easily
done oropharyngeal decontamination with a 0.12%
chlorhexidine oral rinse significantly reduced the
nosocomial respiratory infection rate and mortality
in a comparatively homogeneous population of
adults undergoing heart surgery.
Unfortunately, little is known about the effects
of oral care interventions in critically ill children.
Evidence-based protocols for oral care for these chil-
dren are not available, and oral hygiene measures are
generally directed toward a patient’s comfort rather
than removal of microbes. Thus, the purpose of our
study was to analyze the oropharyngeal microbio-

320 AJCC AMERICAN JOURNAL OF CRITICAL CARE, July 2009, Volume 18, No. 4 www.ajcconline.org
logical colonization profile of children receiving
mechanical ventilation. We used 2 methods of oral
decontamination: mechanical intervention alone
and mechanical intervention plus 0.12% chlorhexi-
dine. We also evaluated the effect of these interven-
tions on the duration of mechanical ventilation and
length of PICU stay.
Methods
Setting and Sample
This prospective, randomized, controlled study
was performed in a PICU in São Paulo, Brazil. The
aims, methods, benefits, discomforts, and potential
risks of the interventions were described to each
child’s parent or responsible adult according to the
recommendations of the Helsinki Declaration. Of
the 146 children admitted to the PICU during the 9
months of the study, 56 (38%) were selected for
participation. Children were not eligible if they
were newborns, fulfilled the Centers for Disease
Control and Prevention criteria for pneumonia in
infants and children at the time of PICU admission,
were in the PICU for less than 48 hours, had a tra-
cheotomy, or if informed consent had not been
granted. A total of 47 intubated children and 9
nonintubated children (ie, those who received
mechanical ventilation for <24 hours) were
enrolled in the study.
The children were assigned randomly to 2 groups.
For the experimental group, oral care included use
of an oral gel containing chlorhexidine digluconate
0.12% as an active ingredient (chlorhexidine diglu-
conate 0.12%; methylcellulose gel 2.12%, 25 g;
gooseberry syrup, 4 drops; menthol solution 50%,
3 drops; and distilled water, to 30 g). The control
group received the same oral care with the use of a
similarly formulated gel without the antiseptic agent.
The gel type was color coded and the nurses had no
knowledge of the type of gel (with or without anti-
septic) until the end of the study. Only the pharma-
cist was aware of the gel type used for each patient.
Procedures
Before the study, all PICU nurses were trained in
oral care by a dentist who used a protocol designed
to remove microorganisms from all mouth surfaces,
including hard and soft tissues. The training
included evaluation of a child’s oral status, selection
of oral care equipment according to the child’s age,
and a description of the desired outcome, preserving
the integrity of oral and labial mucosa.
For each child, before oral care began, the child
was placed in a lateral position to prevent pul-
monary aspiration of secretions. The gel was applied
www.ajcconline.org AJCC AMERICAN JOURNAL OF CRITICAL CARE, July 2009, Volume 18, No. 4
on a toothbrush and the teeth were cleaned in
quadrants; all teeth surfaces were cleaned (vestibu-
lar, lingual, occlusal, and incisal). After each quad-
rant was cleaned, 10 mL of water (dispensed via a
syringe) was used to rinse the quad-
rant and continual aspiration was Little is known
used to remove all the gel and
debris. After all the teeth were about the effects
cleaned, the ventral surface of the
of oral care inter-
tongue was brushed with posterior-
to-anterior movements. A sponge ventions in criti-
swab was then immersed in the gel
and the gel was applied over all cally ill children.
the oral mucosa. During the hygiene process and
rinsing of each mouth quadrant, fluids and secre-
tions were aspirated by using a vacuum aspirator.
The protocol was used twice a day and took about
10 minutes to complete, depending on the child’s
acceptance and clinical conditions. Nurses’ compli-
ance with the oral care protocol during the study
period was evaluated by 2 trained researchers in a
random fashion, and retraining was conducted
when necessary.
Measures
The dependent variables selected for the study
were the profile of oropharyngeal colonization,
duration of mechanical ventilation, and length of
PICU stay. Oropharyngeal colonization was ana-
lyzed by using a qualitative microbiological culture
assay of samples from the tonsillar area and the
upper posterior part of the oropharynx. Samples
were collected during the first 24 hours of PICU
admission (day 0), at 48 hours (day 2), at 96 hours
(day 4), and at the time of discharge from the PICU.
All the secretions were collected by 3 trained
nurses 8 to 10 hours after oral care. A standard
protocol was used for sample col-
lection, storage, labeling, and On study admis-
transport to the laboratory. A sterile
swab plastic stick 15 cm long with a sion, 41% of oral
cotton tip was pressed and rolled samples were col-
on the tonsillar area and the upper
posterior part of the oropharynx to onized with patho-
obtain oropharyngeal secretions.
The swab with the sample secretions
genic bacteria.
was immersed in a sterile tube containing 5 mL of
Stuart agar. Then the tube was labeled and immedi-
ately transported to the laboratory.
In the microbiological laboratory, the samples
were cultured on blood agar, chocolate agar, eosin–
methylene blue agar, and Sabouraud agar, and incu-
bated according to controlled atmosphere, tempera-
ture, time, and humidity parameters for qualitative
321
 Table 1
Baseline characteristics of the sample

Groupa
determined by comparing the size of the halos
with the established standards.22
Control Experimental
Characteristic (n = 29) (n = 27) P
The following antibiotics were used in the sen-
sitivity analyses, as determined by the pattern
Age, mean (SD), y 3.0 (3.9) 1.6 (5.2) .85b established in the hospital for the years 2005 and
2006: amikacin, tobramycin, gentamicin, cefepime,
Male sex 18 (62) 17 (63) .94c
ceftazidime, ciprofloxacin, imipenem, meropenem,
Nutritional condition piperacillin, disodium clavulanate, polymyxin, cef-
Normal 18 (62) 10 (37)
Malnutrition 10 (34) 16 (59) .16c
triaxone, and sulfamethoxazole plus trimethoprim.
Overweight 1 (3) 1 (4) Duration of mechanical ventilation (in hours)
and length of PICU stay (in days) were determined.
Emergency admission to hospital 17 (59) 12 (44) .29c
Other data collected included each patient’s age;
Emergency admission to PICU 16 (55) 13 (48) .60c sex; nutritional status according to a Z score (nor-
Preexisting chronic conditions 19 (65) 21 (78) .31c mal, malnutrition, overweight); clinical evaluation
Underlying disease of the condition of the oral mucosa (presence or
Surgical 16 (55) 15 (56) .98c absence of alterations such as moniliasis, gingivitis,
Clinical 13 (45) 12 (44) and injuries); oral health status according to the
Presence of infection at admission 17 (59) 20 (74) .22c DMFT (decayed, missing due to caries, and filled
Antibiotic therapy before admission 13 (45) 8 (30) .24c
teeth) index, previous hospital length of stay; pres-
ence of infectious or chronic disease at admission;
NEMS, mean (SD) 26.2 (8) 24.6 (7.7) .41d
use of antibiotics; type of admission (elective or
Intubation 26 (90) 21 (78) .29d emergency); diagnoses (clinical or surgical); Nine
Oral route 26 (100) 21 (100) Equivalents of Nursing Manpower Use Score; use of
Emergency intubation 10 (38) 7 (33) .72c
Uncuffed tubes 16 (62) 13 (62) >.99c
drugs that could affect oropharyngeal colonization
Duration of mechanical 84.0 (120) 96.0 (147.4) .67d (central nervous system suppressors, salivary secre-
ventilation, mean (SD), h tion modifiers, immunological suppressors, gastric
Enteral tubes 12 (41) 13 (48) .71c pH modifiers); characteristics of intubation, includ-
ing indication (emergency and elective), type (oral
Medications used during PICU stay
Central nervous system suppressors 27 (93) 21 (78) .14e
or nasal), and type of endotracheal tube (cuffed or
Salivary secretion modifiers 16 (55) 14 (52) .80c uncuffed); presence of enteral tubes; and outcome
Immunological suppressors 11 (38) 10 (37) .94c (discharge or death). All patients were followed up
Gastric pH modifiers 28 (97) 24 (89) .34e until discharge from the PICU.
Normal DMFT index 28 (97) 24 (89) .34e Categorical variables were evaluated by using
No alteration of oral mucosa 27 (93) 23 (85) .41e
χ2 and Fisher exact tests. Numerical variables were
evaluated by using a t test or analysis of variance.
Length of PICU stay, mean (SD), d 6 (4.4) 6.1 (7.3) .22e
Rejection of the null hypothesis was set at α = .05.

Abbreviations: DMFT, decayed, missing due to caries, filled teeth; NEMS, Nine Equiv-
alents of Nursing Manpower Use Score; PICU, pediatric intensive care unit.
a Values are expressed as number (%) of children unless otherwise indicated.
b By t test.
c By χ2 test.
d Mann-Whitney test.
e Fisher exact test.
microbiological identification. After incubation,
growth of colonies was evaluated by 2 microbiolo-
gists, and analyses of microbial resistance to antibi-
otics were done. The diffusion disk technique with
Mueller-Hinton agar was used for qualitative analy-
ses. Length of incubation, ionic concentration, tem-
perature, nutritional characteristics of the plaque,
incubation, and application of the antibiotics disks
to be tested were done in accordance with the rec-
ommendations of the Clinical and Laboratory Stan-
dards Institute.22 Sensitivity and resistance were
Results
Characteristics of the Sample
Overall, 56 children were enrolled: 29 (52%)
in the control group and 27 (48%) in the experi-
mental group. At baseline, both groups had simi-
lar demographic characteristics, preexisting
medical conditions, underlying diseases, and
pharmacological and nutritional support. The
characteristics of intubation did not differ signifi-
cantly between the groups. Most of the patients
had infectious disease at the time of PICU admis-
sion. The 2 groups did not differ in the Nine
Equivalents of Nursing Manpower Use Score, clin-
ical conditions of the oral cavity according to the
DMFT index, health status of the oral mucosa,
mean duration of mechanical ventilation, or
mean length of PICU stay (Table 1).

322 AJCC AMERICAN JOURNAL OF CRITICAL CARE, July 2009, Volume 18, No. 4 www.ajcconline.org
 80 P = .52b

Cultures positive for pathogenic microflora, %

P= .38a
Oropharyngeal Colonization 70
Because of discharge (control group, 85%; exper-
imental group, 81%) and death (control group, 15%; 60
experimental group, 19%), sequential samples of
50 P = .62a
oropharyngeal samples were obtained from 56 P = .72a
patients on day 0, from 52 on day 2, from 31 on
40
day 4, and from 9 at PICU discharge. The effects of
the experimental intervention on colonization by 30
pathogenic (Staphylococcus aureus, Klebsiella pneumo-
niae, Enterobacter species, Pseudomonas aeruginosa, 20
Acinetobacter baumannii, Proteus mirabilis, Morganella
morganii) and nonpathogenic (Streptococcus viridans, 10
coagulase-negative staphylococci, Moraxella species)
0
microorganisms are presented in the Figure.
On admission, overall 84% (control group, 86%; 0 2 4 PICU discharge
experimental group, 85%) of oropharyngeal samples Time, days
contained normal flora, and 41% (control group, 38%;
P = .25b
experimental group, 44%) contained pathogenic flora. P = .72b
The frequency of oropharyngeal colonization by Cultures positive for normal microflora, %
P = .43b P > .99b
normal flora (P = .72) and pathogenic flora (P = .62) 80
did not differ significantly between the 2 groups.
During the first 48 hours of PICU admission,
the number of children colonized with pathogenic 60
microorganisms decreased in the experimental group
and increased in the control group. Table 2 gives
the number of children colonized and the microor- 40
ganisms identified.
Streptoccocus viridans was detected in most of
the samples in both groups. Coagulase-negative 20
staphylococci and Moraxella species were detected
more often in the experimental group than in the
control group. Overall, gram-negative bacteria were 0
the predominant species. The frequency of A bau- 0 2 4 PICU discharge
mannii and P aeruginosa was higher in the control
Time, days
group than in the experimental group, and that of
K pneumoniae and Enterobacter species was higher in Control Experimental
the experimental group (Table 2).
A total of 26 samples contained pathogenic bacte-
ria, and 24 (92%) of the 26 were antibiotic resistant, Figure Percentage of cultures positive for pathogenic and nor-
mal microorganisms in samples of oropharyngeal secretions from
such as K pneumoniae strains resistant to β-lactamase,
children treated with toothbrushing alone (control group) or with
methicillin-resistant S aureus, carbapenem-resistant toothbrushing plus 0.12% chlorhexidine (experimental group).
P aeruginosa and A baumannii, and cephalosporin- Abbreviation: PICU, pediatric intensive care unit.
resistant Enterobacter species (Table 3). a By χ2 test.

The effects of chlorhexidine on oropharyngeal b Fisher exact test.

colonization are shown in the Figure and Table 4.

Colonization by pathogenic bacteria did not differ
between the 2 groups of children. From day 0 to
day 2, the number of children with an increase in
the number of samples positive for pathogenic flora
was greater in the control group than in the experi-
mental group, but the difference was not significant.
Similarly, the colonization of the oral cavity by nor-
mal flora did not differ between the 2 groups of
children (Figure and Table 4).
Discussion
The oral cavity can be a site of origin for dis-
semination of pathogenic organisms to distant body
sites, such as the lungs.23 The Centers for Disease
Control and Prevention have suggested that noso-
comial respiratory infections are due to 4 methods
of inoculation: aspiration of oropharyngeal organ-
isms, inhalation of aerosols containing bacteria,

www.ajcconline.org AJCC AMERICAN JOURNAL OF CRITICAL CARE, July 2009, Volume 18, No. 4 323
 Table 2
Microbiological profile of cultures of
oropharyngeal secretions from critically ill children
In a systematic review and meta-analysis of the
in a pediatric intensive care unit (PICU), by group studieda
effect of oral decontamination, with antiseptics or
Day
antibiotics, on the incidence of VAP and mortality in
PICU
Microorganism 0 2 4 discharge adults receiving mechanical ventilation, Chan et al24
found that oral decontamination with antiseptics
Control samples (n = 29) (n = 27) (n = 16) (n = 5) was associated with a lower risk for VAP. However,
neither antiseptic nor antibiotic oral decontamina-
Normal flora
Streptococcus viridans 25 (86) 21 (78) 10 (62) 4 (80)
tion reduced mortality, duration of mechanical ven-
Coagulase-negative 10 (34) 6 (22) 1 (6) 0 tilation, or length of ICU stay.
staphylococci
Moraxella species 9 (31) 5 (19) 1 (6) 0 Oropharyngeal Colonization
Pathogenic flora We found a high rate of oropharyngeal coloniza-
Staphylococcus aureus 4 (14) 4 (15) 5 (31) 1 (20) tion in PICU patients. During the first 24 hours of
Klebsiella pneumoniae 1 (3) 2 (7) 1 (6) 0 PICU admission, the oropharynx was colonized by
Enterobacter species 1 (3) 1 (4) 1 (6) 0
aerobic pathogens in 40% of the children. In addi-
Pseudomonas aeruginosa 0 1 (4) 3 (19) 1 (20)
Acinetobacter baumannii 3 (10) 3 (11) 1 (6) 0 tion, some of these children had colonization by
Proteus mirabilis 1 (3) 1 (4) 1 (6) 0 multidrug-resistant pathogens. Four days after admis-
Klebsiella oxytoca 0 0 0 1 (20) sion, more than 50% had colonization by bacterial
Morganella morganii 1 (3) 0 0 0 pathogens. We found no significant differences
Experimental samples (n = 27) (n = 25) (n = 15) (n = 4) between the 2 groups in colonization characteris-
Normal flora tics. These results were similar to those of Fourrier
S viridans 20 (74) 20 (80) 9 (60) 3 (75) et al25 in a study of critically ill adults receiving
Coagulase-negative 9 (33) 6 (24) 7 (47) 0 mechanical ventilation. Approximately 50% of the
staphylococci patients had cultures positive for bacterial pathogens
Moraxella species 7 (26) 10 (40) 4 (27) 0
at admission, and 33% of these patients had aero-
Pathogenic flora bic pathogens, mainly gram-negative bacteria.25
S aureus 3 (11) 2 (8) 2 (13) 0 In our study, the aerobic gram-negative bacte-
K pneumoniae 3 (11) 3 (12) 3 (20) 1 (25)
Enterobacter species 3 (11) 3 (12) 2 (13) 1 (25)
ria identified most frequently were P aeruginosa,
P aeruginosa 2 (7) 2 (8) 1 (7) 1 (25) Escherichia coli, K pneumoniae, and various species
A baumannii 1 (11) 0 0 0 of Acinetobacter. The number of infections caused
Escherichia coli 2 (7) 1 (4) 1 (7) 0 by gram-positive bacteria is increasing rapidly in
M morganii 1 (11) 0 0 0 adult ICUs, particularly infections caused by methi-
a
cillin-resistant strains of S aureus. The incidence of
Values are expressed as number (%) of children colonized.
VAP related to multidrug-resistant pathogens has
also increased, because of indiscriminate use of
hematogenous spread from distant body sites, and antibiotics, prolonged hospitalization, high fre-
bacterial translocation from the gastrointestinal quency of antibiotic resistance in the community,
tract.9 Of these 4, aspiration is thought to be the most and immunosuppression.2,3
important. Thus, a reduction in the oropharyngeal Children in the experimental group had more
microbial flora would theoretically species of Enterobacteriaceae, such as Enterobacter
have a marked effect on oral colo- species (75%), E coli (100%), and K pneumoniae
Pathogenic nization and the occurrence of respi- (71%), than did children in the control group. Sim-
ratory nosocomial infections.21 ilar findings were obtained in another study1 in
colonization We found no difference between which treatment with chlorhexidine caused a
decreased in the the control and experimental groups greater reduction in gram-positive bacteria than in
in colonization by pathogenic bac- gram-negative organisms.
chlorhexidine group teria. Fewer children in the experi- Dental plaque is due to bacterial colonization
and increased in mental group had an increase from of the surfaces of teeth, soft tissues, and dental
day 0 to day 2 in the number of prostheses via selective adherence mechanisms.
the control group. samples positive for growth of path- Dental plaque is a biofilm, a dynamic and complex
ogenic microorganisms, but the dif- system that contains microorganisms embedded in
ference was not significant. Similarly, colonization an extracellular matrix. Plaque mass increases by
of the oral cavity by normal flora did not differ cumulative addition of aerobic, anaerobic, and fila-
between the 2 groups. mentous microorganisms. Numerous factors are

324 AJCC AMERICAN JOURNAL OF CRITICAL CARE, July 2009, Volume 18, No. 4 www.ajcconline.org
 Table 3
Pathogenic microorganisms’ resistance according to groupa
Day 0 Day 2 Day 4 PICU discharge
Pathogen Control Experimental Control Experimental Control Experimental Control Experimental

Staphylococcus aureus 4 (100) 3 (100) 3 (100) 2 (100) 4 (100) 3 (100) 1 (100) 0

Methicillin-resistant 1 (25) 2 (67) 1 (33) 1 (50) 1 (25) 1 (33) 1 (100) 0
Klebsiella pneumoniae 1 (100) 3 (100) 2 (100) 3 (100) 1 (100) 3 (100) 0 1 (100)
ESBL producer 0 2 (67) 0 2 (67) 0 2 (67) 0 1 (100)
Enterobacter species 1 (100) 3 (100) 1 (100) 3 (100) 1 (100) 2 (100) 0 1 (100)
Cephalosporin-resistant
Second-generation 1 (100) 0 1 (100) 0 1 (100) 0 0 0
Third-generation 0 1 (33) 0 1 (33) 0 0 0 0
Pseudomonas aeruginosa 0 2 (100) 1 (100) 2 (100) 3 (100) 1 (100) 1 (100) 1 (100)
Carbapenens-resistant 0 0 0 0 0 0 1 (100) 0
β-lactamase inhibitor 0 2 (100) 1 (100) 2 (100) 1 (33) 1 (100) 0 1 (100)
resistant
Acinetobacter baumannii 3 (100) 1 (100) 3 (100) 0 1 (100) 0 0 0
Carbapenens-resistant 3 (100) 0 3 (100) 0 1 (100) 0 0 0
β-lactamase inhibitor 0 1 (100) 0 0 0 0 0 0
resistant

Abbreviations: ESBL, extended-spectrum β-lactamase; PICU, pediatric intensive care unit.

a Values are expressed as number (%) of samples.

involved in the development of plaque; however,

Table 4
poor oral hygiene and lack of mechanical elimi- Changes in colonization by normal
nation of microorganisms are the main factors and pathogenic floraa
leading to proliferation and accumulation of
Period
dental plaque and subsequent colonization.26
Adherent streptococci drench the salivary Day 0 to Day 2 to Day 4 to
pellicle on binding sites during the first 2 to 8 Change day 2 day 4 discharge
hours of plaque deposition. This growth period
Normal flora
is independent of personal characteristics, sur- Control group
face, and time and appears to depend on cell Decrease 5 (19) 4 (29) 1 (33)
density. Initial colonization of enamel surfaces Increase 10 (38) 3 (21) 1 (33)
by bacteria occurs in 3 stages: saturation of pel- No alteration 11 (42) 7 (50) 1 (33)
Experimental group
licular binding sites, accumulation of organisms
Decrease 9 (38) 5 (36) 0
via a variety of mechanisms until a critical den- Increase 3 (12) 4 (29) 2 (50)
sity is reached, and density-dependent growth.27 No alteration 12 (50) 5 (36) 2 (50)
Several studies1,25,26 have suggested that Pb .09 .74 .46
oropharyngeal colonization plays an important
Pathogenic flora
role as a reservoir of nosocomial colonization
Control group
and support the hypothesis that antiseptic decon- Decrease 4 (27) 2 (15) 2 (50)
tamination of dental plaque might decrease the Increase 5 (33) 4 (31) 1 (25)
rate of acquired nosocomial infection in ICU No alteration 6 (40) 7 (54) 1 (25)
adult patients. However, few data support this Experimental group
Decrease 3 (27) 1 (12) 2 (67)
hypothesis for infants and children, and we
Increase - 2 (25) 0
found that in children in a PICU, the effects of No alteration 8 (73) 5 (62) 1 (33)
oral care consisting of mechanical intervention
Pb .08 .93 .65
plus chlorhexidine did not differ from the
a Values are expressed as number (%) of samples.
effects of oral care consisting of mechanical b By χ2 test.
intervention alone.

www.ajcconline.org AJCC AMERICAN JOURNAL OF CRITICAL CARE, July 2009, Volume 18, No. 4 325
 Chlorhexidine
Chlorhexidine increases the permeability of bac-
terial cell walls in a dose-dependent manner by inter-
acting with anionic receptors on the bacterial surface.15
Caton et al28 found that rinsing with chlorhexidine
solution before mechanical cleaning had a profound
and sustained effect on the aerobic and facultative
flora of the oral cavity and may contribute to a variety
of clinical benefits. A meta-analysis29 of the efficacy of
topical chlorhexidine for prevention
of VAP indicated that topical
A total of chlorhexidine is beneficial in prevent-
92.3% of the ing VAP and that the benefit is most
marked in cardiac surgery patients.
pathogenic To document the effect of antisep-
bacteria were tic decontamination of gingival and
dental plaque on the rate of nosoco-
antibiotic-resistant mial bacteremias and respiratory infec-
tions acquired in the ICU, Fourrier et
strains. al26 carried out a prospective, multicen-
ter, double-blind, placebo-controlled efficacy study. A
total of 228 edentulous adults requiring endotracheal
intubation and mechanical ventilation had 0.2%
chlorhexidine gel or a placebo gel applied to gingival
and alveolar processes 3 times a day. Compared with
the control group, patients treated with chlorhexidine
had fewer dental plaque cultures that remained nega-
tive for bacterial growth or became negative after 5
days, but the difference was not statistically significant.
In our study, chlorhexidine influenced the growth of
both normal flora and pathogenic flora, decreasing
the number of microorganisms in cultures of oropha-
ryngeal secretions mainly after 2 days of oral care,
but the results were not significant.
The number of chlorhexidine applications in our
study (2/d) differed from the number in the study of
Fourrier et al26 (3/d). Although this variation may be
important, other investigators30 found no direct rela-
tionship between time interval and the development
of biofilms. The characteristics of the
No difference microflora in children may be relevant
for the chlorhexidine effect. Sharma et
was found in al31 concluded that in children 13 to
colonization 14 years old, a once-a-day unsuper-
vised toothbrushing had the same
between groups effect on plaque formation as did a
twice-daily mouth rinsing with 0.2%
by pathogenic chlorhexidine. In our study, all treat-
bacteria species. ments were performed twice a day in
all children for several reasons, includ-
ing better compliance with the protocol, lack of defin-
itive evidence to determine the most appropriate
method of oral hygiene, and lack of knowledge about
the effects of chlorhexidine in young children.32,33
326 AJCC AMERICAN JOURNAL OF CRITICAL CARE, July 2009, Volume 18, No. 4
Studies21,25,26,34 on the effects of oral chlorhexidine
have yielded conflicting results. In a meta-analysis,
Pineda et al34 did not find any clinical benefits of
regular oral application of chlorhexidine on the inci-
dence of nosocomial pneumonia and mortality rate
in critically ill patients requiring mechanical ventila-
tion. Fourrier et al25 investigated the effect of antisep-
tic decontamination of dental plaque on plaque
colonization by aerobic pathogens and nosocomial
infections in 60 adult patients receiving mechanical
ventilation. In that study, antiseptic decontamination
with a 0.2% chlorhexidine gel decreased dental bac-
terial colonization on day 5 to 7 after admission,
but the effect did not persist after 10 days.
In an in vitro model,35 the effect of chlorhexi-
dine was time dependent, and exposure times of
30 seconds had little effect on the number of viable
bacteria recovered from oral biofilms. Even at 0.2%,
chlorhexidine was ineffective against dental plaque
after 5 minutes of exposure and required 60 min-
utes to achieve an effective killing. Therefore, one
reason for the lack of effect of our experimental
protocol may be insufficient contact time with bac-
teria; increased contact times might be effective.
Another key point is microbial resistance. Irizarry
et al36 reported that antibiotic-resistant microorgan-
isms had a reduced susceptibility to antiseptic and
disinfectant agents such as chlorhexidine. Biocide
resistance among microorganisms has been consid-
ered an important clinical issue.37 In a study by Suller
and Russell38 reported in 1999, the minimal inhibitory
concentration of chlorhexidine for methicillin-
resistant S aureus was 1.5- to 3-fold greater than
that for methicillin-sensitive S aureus.
In a recent study, Vali et al39 observed reduction
in susceptibility of pathogens to chlorhexidine, and
therefore reduced microbial susceptibility to bio-
cides may be a serious concern in clinical practice.
Clinical studies24,28,29 involving critically ill
patients have shown that inadequate salivary flow
promotes the development of pharyngeal mucositis
and increased colonization by aerobic pathogens.
The presence of endotracheal or feeding tubes con-
tributes to the formation of biofilms strongly resist-
ant to antiseptics or antibiotics. Isolates from the
initial samples in our study had high indices of
antibiotic resistance; therefore, these isolates may
have been less susceptible to the effects of chlorhex-
idine than antibiotic-sensitive isolates would be.
Toothbrushing
The lack of significant differences in our study
may be related to the mechanical intervention of
toothbrushing. Use of a toothbrush is widely con-
www.ajcconline.org
sidered to be the only effective means to remove
dental plaque, but toothbrushing is not widespread
in orally intubated children. To the best of our
knowledge, no investigators have evaluated the effect
of oral care with pharmacological and mechanical
interventions in critically ill children. Thus, compar-
isons of our results with results from adult popula-
tions are difficult. Furthermore, a direct comparison
between adults and children may be difficult because
of the lack of knowledge of differences in oropharyn-
geal colonization in these 2 groups.
Study Limitations
This study was limited by a small sample for all
4 time points. Conversely, the results do provide
unique, preliminary data on oral care in children
receiving mechanical ventilation, suggesting that
toothbrushing alone can be as effective as tooth-
brushing plus a pharmacological intervention to con-
trol overgrowth of oropharyngeal pathogens in PICU
patients. Future research should address issues such
as the effect of oral care on the development of VAP
in children; depending on the results, the use of oral
care protocols may be an important part of achieving
evidence-based care in critically ill children.
Conclusion
The addition of a pharmacological intervention
to oral care in critically ill children did not change
the profile of microorganisms that colonized the
oropharynx, duration of mechanical ventilation, or
length of PICU stay.
ACKNOWLEDGMENTS
This research was done at the Nursing School, Federal
University of São Paulo.
FINANCIAL DISCLOSURES
This research was supported by grant 04-13361-2, Fun-
dação de Amparo a Pesquisa do Estado de São Paulo.
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CE Test Test ID A091804: Oral Care Interventions and Oropharyngeal Colonization in Children Receiving Mechanical Ventilation. Learning
objectives: 1. Describe the incidence of ventilator-associated pneumonia in the pediatric intensive care unit (PICU) patient population. 2. Identify microorgan-
isms that commonly colonize the oropharynx of PICU patients. 3. Recognize the impact of an oral care routine using chlorhexidine on a PICU study group.
1. According to results from the US National Nosocomial Infections 6. What was the predominant species detected in oropharyngeal
Surveillance System, ventilator-associated pneumonia accounts for samples obtained from patients during the study?
what percentage of nosocomial infections in infants less than 2 months a. Gram-negative bacteria
old? b. Gram-positive bacteria
a. 20% c. 26% c. Coagulase-positive bacteria
b. 18% d. 21% d. Coagulase-negative bacteria

2. Which of the following may occur when patients receiving mechani- 7. What was the mean average length of PICU stay for children in the
cal ventilation have decreased salivary secretions and poor oral cavity control sample of the study?
hygiene? a. 27 days c. 4.4 days
a. Tissue necrosis b. 6 days d. 12 days
c. Bacterial overgrowth
b. Periodontal disease 8. What percentage of children in the study group showed Staphylococcus
d. Gingivitis aureus in a control sample on study day 0 in a microbiological prof ile of
cultures of oropharyngeal secretions?
3. Which of the following 2 techniques have been described in studies a. 14% (4 children) c. 31% (5 children)
as effective methods for removing dental plaque and associated b. 15% (4 children) d. 20% (1 child)
microbes in critically ill patients?
a. Mechanical intervention and direct pharmacological intervention with 9. What effect does chlorhexidine have on bacterial cell walls?
antimicrobial agents a. Decreased permeability c. Increased permeability
b. Preventing tracheal and esophageal aspirate b. Increased osmotic pressure d. Decreased osmotic pressure
c. Hand hygiene with alcohol gel and nasopharyngeal suctioning
d. Patient positioning and oral suctioning 10. Which of the following treatments contributes to the formation of
biof ilms strongly resistant to antiseptics?
4. Which of the following statements best describes the effects of oral a. Frequent oropharyngeal suctioning
care interventions in critically ill children? b. Administration of total parental nutrition
a. Clorhexidine oral rinse significantly reduces the incidence of nosocomial c. Immunosuppressant therapy
respiratory infection. d. Endotracheal intubation
b. Using mouthwash and a toothbrush for oral hygiene had no influence on
the rate of nosocomial infection. 11. What action is widely considered to be the only effective means to
c. Little is known about the effects of oral care interventions in critically ill remove dental plaque?
children. a. Maintaining mouth moisture
d. Adult oral care evidence-based practices are equally effective in critically ill b. Using a toothbrush
children. c. Using dental floss
d. Removing oral secretions
5. Which of the following microorganisms was most frequently detected in
study samples from both the control group and the experimental groups? 12. What conclusion did the investigators make after adding a pharma-
a. Coagulase-negative staphylococci cological intervention to oral care in critically ill children?
b. Moraxella species a. The oropharyngeal colonization of resistant bacteria decreased.
c. Acinetobacter baumannii b. The length of PICU stay decreased.
d. Streptococcus viridans c. The duration of mechanical ventilation decreased.
d. There was no change in oropharyngeal colonization of microorganisms.
Test ID: A091804 Contact hours: 1.5 Form expires: July 1, 2011. Test Answers: Mark only one box for your answer to each question. You may photocopy this form.
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Kc Kc Kc Kc Kc Kc Kc Kc Kc Kc Kc Kc
Kd Kd Kd Kd Kd Kd Kd Kd Kd Kd Kd Kd
Fee: AACN members, $0; nonmembers, $11 Passing score: 9 Correct (75%) Category: A Synergy CERP A Test writers: Deborah Lilly, RN, MSN, CCRN
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