LITERATURE REVIEW

doi: 10.1111/nicc.12002

A review of oral preventative

strategies to reduce
ventilator-associated pneumonia
Tom Andrews and Colin Steen
ABSTRACT
Aim: This article evaluates the evidence for and efficacy of the use of mechanical hygiene and chlorhexidine in the prevention of
ventilator-associated pneumonia (VAP).
Search strategies: Inclusion criteria: primary research articles; randomized controlled trials; systematic reviews. Exclusion criteria: quasiexperimental trials; opinion articles. Search Engines: PubMed; CINAHL; and EBSCO.
Background: VAP is the commonest infection found in critically ill patients who are mechanically ventilated. It is associated with increased
mortality, increased length of stay in intensive care and increased costs.
Relevance to clinical practice: VAP is a health care-associated infection consistent with the presence of an endotracheal tube and
mechanical ventilation for greater than 48 h. Efforts aimed at reducing infection rates include oral decontamination and mechanical hygiene to
control the bacteria responsible, since there is an association between changes in bacteria found in the oropharynx and its development. Tooth
brushing and the use of an oral antiseptic such as chlorhexidine gluconate are increasingly recommended in ventilator care bundles.
Conclusion: While there have been a number of studies conducted evaluating the efficacy of both approaches, there is limited evidence to
support their use. The frequency of oral decontamination and mechanical hygiene interventions have not been established and chlorhexidine
2% seems to be more effective compared to weaker concentrations, but data is mainly confined to patients following cardiothoracic surgery.
Key words: chlorhexidine gluconate critical care nursing effectiveness of health care intervention infection prevention oral care oral decontamination oral
hygiene tooth brushing ventilator-associated pneumonia

INTRODUCTION
An accurate diagnosis of ventilator-associated pneumonia (VAP) remains a challenge, with no consensus
on a reference definition (CDC, 2012; Hunter, 2012).
VAP is usually suspected if the patient was intubated
and ventilated at the time or within 48 h before the onset
of ventilation and uses a combination of radiological,
clinical and laboratory criteria (CDC 2012). However,
this definition is under review because of its subjectivity and complexity and any new definition is likely to
differentiate between a ventilator-associated condition
and an infection-related ventilator-associated complication (CDC, 2012). The incidence of VAP ranges from

Authors: T Andrews, RN, BSc (Hons), MSc, PhD, School of Nursing and
Midwifery, University College Cork, Cork, Ireland; C Steen, RN, BSc
(Hons), MSc, School of Nursing, Midwifery and Social Work, University of
Manchester, Manchester, UK
Address for correspondence: T Andrews, School of Nursing and
Midwifery, Brookfield Health Science Complex, University College Cork,
College Road, Cork, Ireland
E-mail: t.andrews@ucc.ie

116

10% to 30% (Labeau et al., 2011) with a crude mortality that may exceed 50% and is associated with
increased prolonged intensive care and hospital stay,
increased cost and delays in recovery (Scannapieco
et al., 2003; Vincent, 2003; Chan et al., 2007; Chan et
al., 2007). However, the attributable mortality, defined
as the total mortality minus the mortality associated
with the underlying disease process (Muscedere et
al., 2010), may be much lower, somewhere in the
region of 44% (Bekaert et al., 2011) to an absolute
attributable mortality of 135% (Muscedere et al., 2010).
Methodological issues such as the heterogeneity in
studies, the associated mortality of the underlying disease and the absence of a reference standard for VAP
make assessment of attributable mortality challenging
(Muscedere et al., 2010; Bekaert et al., 2011). The cost
of VAP has been estimated as between 9000 and
31 000 (Daz et al. 2009). In critically ill patients and
especially those who are mechanically ventilated, oral
flora changes from predominantly Viridans streptococci, Haemophilus species and anaerobes (Chlebicki

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Oral hygiene preventative strategies

and Safdar, 2007) to a predominance of aerobic Gramnegative bacilli and Staphylococcus aureus predisposing
them to the development of VAP (Safdar et al., 2005).
The most important mechanism in the development of
VAP is aspiration of oropharyngeal organisms into the
distal bronchi (Chlebicki and Safdar, 2007).
The prevention of VAP needs to address three
primary issues: aspiration, aerodigestive tract colonization and contaminated equipment (Rebmann and
Greene, 2010). Part of that approach is the implementation of a comprehensive oral hygiene programme.
Two possible options for reducing the incidence of VAP
include selective digestive decontamination (SDD) and
selective oral decontamination (SOD) using oral antiseptics. In SDD, non-absorbable antibiotics are administered topically through the oral cavity and nasogastric
tubes to reduce the bacterial load in the upper GI and
buccal cavity and is combined with a short course
of intravenous antibiotics. This is based on the contention that the stomach is an important reservoir of
bacteria that cause VAP (Safdar et al., 2005). Prophylaxis includes parenteral and enteral antimicrobials
administration, and hygiene, combined with surveillance cultures of throat and rectal swabs to monitor the
efficacy and compliance of enteral antimicrobials, and
is termed the full four-component protocol of SDD (Silvestri et al., 2009). This treatment has received mixed
reviews. There is evidence that it reduces bacteria
load but it may also lead to antibiotic-resistant bacteria (CDC, 2003). However, previous meta-analyses
of SDD using a combination of topical and systemic
prophylactic antibiotics found a significant reduction
in rates of VAP among treated patients (Liberati et al.,
2009), while a systematic review found that the use of
the full protocol reduced overall mortality in critically
ill patients (Silvestri et al., 2009). Localized SOD in the
form of bactericidal medication to the buccal cavity
has also received mixed results for similar reasons and
further research is required into both these treatment
strategies (National Institute for Clinical Excellence,
2008). Other recommendations include elevated head
of the bed, subglottic secretion drainage and closed
endotracheal suctioning (Muscedere et al., 2008).
An alternative strategy to SDD is oral decontamination and effective oral hygiene. They may be thought
of as a continuum from the use of antibiotics, antiseptics, such as chlorhexidine and povidone-iodine
through to the use of toothbrushes alone and combinations thereof. The CDC (2003) stated that planned,
structured oral hygiene programmes will reduce the
rate of nosocomial pneumonia in ventilated intensive
care patients (Schleder et al., 2002). They advocate a
combined approach of frequent tooth brushing and
the use of antiseptics. They also recommend the use of

subglottic suctions to clear the oropharynx of pooled

secretions. Recent guidelines recommend that all ventilator care bundles include oral antisepsis (NICE,
2008). The use of antiseptics is shown to be more
effective in targeting localized sites and is not associated with the same incidence of bacterial resistance as
drug therapy (Chan et al., 2007). Antiseptics are broad
spectrum antibacterial agents that control plaque formation and inhibit the growth of bacteria (Grap et al.,
2004), as opposed to antibiotics which are bactericidal. In addition to the use of antiseptics, mechanical
tooth brushing is also a method to reduce bacteria in the buccal cavity. There are various methods
of providing oral care including the use of sponge
swabs, toothbrushes, electric as well as manual and the
more advanced suction toothbrush. This article will
evaluate the efficacy of mechanical hygiene and oral
decontamination in reducing the incidence of VAP.
While oral care is considered by nurses as important
and is prioritized, it is perceived as a difficult and
unpleasant task, with oral status deteriorating irrespective of interventions (Binkley et al., 2004; Rello
et al., 2007).

SEARCH STRATEGIES
The following inclusion criteria were used: primary
research articles; randomized controlled trials (RCTs);
systematic reviews; limited from 2007 to 2012. Exclusion criteria: quasi-experimental trials; opinion articles.
The following electronic data bases were searched
using combinations of the keywords oral hygiene,
oral care, oral decontamination, VAP, chlorhexidine
and tooth brushing, PubMed, CINAHL, EBSCO and
EMBASE. This yielded a total of six systematic reviews,
two meta-analyses, two papers which claimed to be
both and four RCTs which were primarily used in this
literature review.

MECHANICAL HYGIENE
Tooth brushing is recommended as the first stage
in an oral hygiene regime to loosen dental plaque
and mechanically remove it with the secondary effect
of reducing the protective biofilm generated by the
bacteria residing there. Subsequent treatment using
antiseptics may follow to combat the bacterial loading.
Oropharyngeal suctioning and other VAP preventative
strategies may also help in the reduction of VAP.
Regular oral hygiene has only a minimal effect on
reducing plaque (Jones et al., 2011).
Patients arrive in critical care units with preexisting oral hygiene issues including high levels of
dental plaque (Jones et al. 2011). This predisposes

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to the development of VAP as plaque is bacteria

laden. The first to identify the link between oral
hygiene and VAP was Scannapieco et al. (1992).
They determined that the rate of dental plaque
and/or buccal cavity colonization by bacteria was
significantly higher in intensive care patients than
those who attended a dental clinic. In subsequent
comparison between tracheal aspirate cultures and
dental plaque, Scannapieco et al. (1992) demonstrated
a correlation between the two suggesting that the
bacteria which grow on dental plaque contribute to
the colonization of the respiratory tract proposing
that dental plaque could be an important reservoir
for bacterial growth (Fourrier et al., 2000). Jones et al.
(2011) further support the findings of Scannapieco
et al. (1992). In a prospective study Fourrier et al.
(2000) examined the incidence of dental plaque in
patients admitted to intensive care, the rate of plaque
growth and the incidence of colonization of the plaque
by bacteria. The bacteria were either present on
admission or developed during patients stay. Over
a 10-day period of data collection there was an increase
in plaque formation and the loading of plaque by
bacteria increased. Similar to Scannapieco et al. (1992),
Fourrier et al. (2000) and later El-Solh et al. (2004)
established a positive correlation between a positive
buccal culture and a significant increase in nosocomial
respiratory infections indicating that bacterial buccal
load may be a source of infection in intensive care
patients.
In a systematic review Scannapieco et al. (2003)
examined the association between periodontal disease
and bacterial pneumonia in high-risk patients such
as those with chronic lung disease and intensive
care patients. They indicated that bacteria grow on
the plaque deposits on teeth and develop a biofilm,
and suggest that this helps to protect them from
topical antiseptic and antibiotic use (El-Solh et al.,
2004; Kishimoto, 2007). They concluded that the data
imply the development of nosocomial pneumonia
in high-risk patients such as intensive care patients
may be linked to poor oral hygiene. They claim that
the incidence of nosocomial pneumonia through the
removal of dental plaque may be reduced by improving
oral hygiene either through mechanical approaches
such as tooth brushing or by chemical means such as
the use of antiseptics.
Kishimoto (2007) advocates the use of tooth brushing
to reduce the incidence of bacteria. Tooth brushing is
more advantageous compared to antiseptic use alone
as tooth cleaning mechanically removes dental plaque,
thus removing the environment that promotes bacterial
growth. It also prevents the development of the
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protective biofilm. This enables subsequent treatment

by antiseptic drug therapies to be more effective.
In a randomized controlled clinical trial, Munro et al.
(2009) examined the effectiveness of chlorhexidine
over tooth brushing. They found that chlorhexidine
significantly reduced the incidence of VAP (p > 0006)
as measured by the clinical pulmonary infection
score (CPIS) whilst tooth brushing had no effect on
development of VAP. The CPIS tool is a method of
determining VAP. It is non-invasive and is dependent
on measurement of physiological variables. There are
criticisms of the CPIS tool in that it is not sensitive as
a predictor of VAP (Zilberberg and Shorr, 2010). The
study mentions the sampling of tracheal aspirate for
culture, but did not report culture outcome. Patients
received other VAP protective strategies which may
have confounded the results.
In a single blinded RCT, Pobo et al. (2009) compared
the effectiveness of electric tooth brushing to standard
oral care on the incidence of VAP and secondary
outcomes such as ventilator free days, length of
stay, antibiotic free days and hospital mortality.
Patients in both study arms received a number of
additional elements that are recommended in the
prevention of VAP, such as head elevation 30 ,
monitoring of endotracheal cuff pressure and stress
ulcer prophylaxis. The study concluded that the use
of electric toothbrush combined with chlorhexidine
mouthwash did not reduce the incidence of VAP.
Utilizing both manual cleaning techniques using
proprietary oral swabs and electric toothbrushes,
and VAP measured via the CPIS tool, in a single
randomized pilot study Yao et al. (2011) determined
that there was a significant reduction in VAP. The
experimental group also received an elevated head
position (3045 ) and oropharyngeal suctioning both
before and after brushing but it is not clear whether
the control group also received these interventions.
In a study by Needleman et al. (2011), two groups
received identical care with the exception of a powered
toothbrush in the experimental group whilst the
control group received oral hygiene with the use
of sponge and no toothbrush. The study intended
to assess the effectiveness of the use of an electric
toothbrush on dental plaque. They concluded that
powered toothbrushes are highly efficient at removing
dental plaque and reducing the pathogens associated
with VAP (p = 0006). They recommend the use of
powered toothbrushes to remove VAP-associated
pathogens and to explore further the direct impact
on the incidence of VAP.
It is not clear from the literature the frequency of
tooth brushing that is required, whether toothpaste
should be used and if so what type and whether

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Oral hygiene preventative strategies

electric tooth brushes are more effective than manual,

since it is generally not made explicit if toothpaste
was used during tooth brushing. The Needleman et al.
(2011) study used chlorhexidine at the time of tooth
brushing whilst Yao et al. (2011) used water. There is
evidence that toothpaste interacts with chlorhexidine
rendering it ineffective and that a separation of 2 h
between the use of tooth brushing and chlorhexidine
rinse is recommended (Kolahi and Soolari, 2006). There
is no consensus in the literature as to the optimal
frequency of tooth brushing for effectively reducing
the incidence of VAP with recommendations ranging
from two (Yao et al., 2011) to four times a day. Further
research is required to establish the frequency and
duration of tooth brushing as well as use and type of
toothpaste.

ORAL DECONTAMINATION
Daily oral care with chlorhexidine has been recently
added to the ventilator care bundle because of its
inhibitory properties on dental plaque formation and
gingivitis and based on recent evidence (Institute for
Health Care Improvement, 2012). It is a pharmacological strategy to control oral colonization by VAP
organisms (Brennan et al., 2004). In Europe, chlorhexidine is widely used by nurses in oral hygiene in the
form of mouthwashes or gels (Jones et al., 2004; Rello
et al., 2007) but less so in the USA, where only 17% of
nurses surveyed used this product (Binkley et al., 2004).
This is likely because the use of an antiseptic agent is
optional in guidelines used for the prevention of VAP
(CDC, 2003) but also because these are not consistently
or uniformly implemented (Cason et al., 2007) and the
optional use of antiseptics in oral hygiene continues
(Johnson et al., 2012).
A meta-analysis of seven RCTs evaluating the
effectiveness of topical chlorhexidine use in reducing
incidences of VAP compared to placebo or standard
care for its prevention, concluded that it is effective
(Chlebicki and Safdar, 2007). Overall the reduction in
VAP was 911% in the treatment group compared
with 1181% in the comparison group. However,
in a sub-group analysis, this effect was seen more
clearly in cardiothoracic patients who accounted for
443 of 805 patients in the studies reviewed. One
explanation for this is that these patients tend to be
intubated and ventilated for a much shorter time. In
one study comprising of 127 patients, a 2% solution
was compared to a usual concentration of 012% or
02%. This could have confounded the results in favour
of the intervention because there is evidence that a
2% solution is much more effective than weaker ones
(Chan et al., 2007).

In a systematic review and meta-analysis of eleven

RCTs totalling 3242 patients, seven trials totalling 2144
patients Chan et al., (2007) evaluated the effectiveness
of antiseptic oral decontamination concluding that
chlorhexidine was not effective in trials using 02%
concentration but was effective at 2%. Similar to
the study by Chlebicki and Safdar (2007), medical
patents derive a more modest effect, suggesting that
specific surgical or trauma patients often have fewer
comorbidities compared to medical or mixed patients.
They suggest that more evidence is needed before
firm conclusions can be made on the full effect of
oral decontamination. This is one of the two studies
relied on by the Institute for Health Care Improvement
(2012) in making recommendations in relation to
chlorhexidine use.
A more recent systematic review and meta-analysis
concluded that there is strong evidence to support
the use of chlorhexidine in the prevention of VAP,
particularly in cardiosurgical patients at 2% but the
protective effect was less strong at lesser concentrations
and in mixed patient population (Labeau et al., 2011).
However, at present the recommended concentration
for use in patients is 012% indicating guidelines
need revision (Institute for Health Care Improvement,
2012). In contrast, Pileggi et al. (2011) showed a
significant (31%) reduction in VAP even using the
lowest concentration of chlorhexidine but with lower
efficacy in non-specialized intensive acre units (ICUs).
However, in this meta-analysis of 28 RCTs, this
was not statistically significant and there was no
overall reduction in mortality. The conclusions from
these systematic reviews and meta-analyses are that
cardiosurgical patients benefit more from the use of
chlorhexidine and that the currently recommended
concentration is likely to be ineffective.
Under the auspices of the Canadian Critical Care
Society comprehensive VAP clinical practice guidelines were developed by carrying out a comprehensive review of RCTs and systematic reviews of RCTs
(Muscedere et al., 2008). The evidence base is only sufficiently strong to indicate that chlorhexidine should be
considered since it may decrease the incidence of VAP.
These were published before the latest meta-analysis.
However, one of the studies that this recommendation
is based on used 2% chlorhexidine as well as bed elevation, making it difficult to conclude that reductions in
the incidence of VAP were due to the use of chlorhexidine alone. In an RCT (Scannapieco et al., 2009) reported
a reduction in the number of S. aureus using chlorhexidine in a concentration of 012% but its use did not
reduce the total number of potential pathogens. Grampositive pathogens such as S. aureus are more sensitive
to chlorhexidine than Gram-negative ones.

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Studies analysing the effectiveness of chlorhexidine

in reducing VAP suffer from a number of methodological issues. There is substantial clinical heterogeneity,
with different patient populations, concentration and
frequency of application of chlorhexidine and definition of VAP (Chlebicki and Safdar, 2007). The effectiveness of 012% chlorhexidine formulations remains
equivocal with studies reporting reductions, absence of
effect as well as increases in anaerobic Gram-negative
bacilli while 012% chlorhexidine formulations at frequencies of up to three times daily appears to be
uniformly ineffective (Lam et al., 2012). Sample sizes
tend to be small and blinding is problematic and often
not reported. While there is some evidence that at
concentrations of 2% chlorhexidine may have some
benefit, patients often receive multi-faceted interventions such as use of the semirecumbent position, stress
ulcer prophylaxis and subglottic drainage which may
confound trial results.

FUTURE DIRECTIONS
The role that biofilm has in the development of VAP
warrants further investigation as it may be a more
significant contributory factor than oropharyngeal
contamination. The evidence that secondary to
colonization with bacteria, endotracheal tubes are
a source of VAP is further supported by evidence
that silver-coated endotracheal tubes significantly
reduce the incidence of VAP (Dallas and Kollef, 2009).
However, more robust clinical trials are needed to
establish the efficacy of such tubes in preventing VAP.
It may be more accurate to refer to the problem not as
VAP but as endotracheal-tube-associated pneumonia
since the problem is the ETT and not the ventilator
(Safdar et al., 2005).
VAP is the most formidable of all infections that are
dealt with in ICU and needs a multi-faceted approach
(Safdar et al., 2005). Combining an antibacterial
approach with something that prevents mucus from
binding to the tube is one such possibility. This is
consistent with the conclusion that the most effective
way to prevent VAP is to decrease the duration of
intubation and mechanical ventilation (Rebmann and
Greene, 2010), more specifically the duration of tracheal
intubation (Hunter, 2012). The most effective claim
that can be made in relation to the routine use of
chlorhexidine is that it shows a decreased trend in the
prevention of VAP but there is evidence that it is more
effective in cardiosurgical patients and at a strength
of 2%. The protective effect is less strong at lesser
concentrations and in mixed patients
There is a trend now of just using chlorhexidine
and assuming that it will fix the problem of
120

oropharyngeal contamination (Safdar et al., 2005).

If oral decontamination is used then it should be
in addition to other evidence-based preventative
measures such as hand hygiene, control of antibiotic
use, strategies that speed up extubation and having
a culture of surveillance (Wiener-Kronish and Dorr,
2008) as well as more specific recommendations
such as those contained in ventilator care bundles.
Although the evidence is not strong, the use of
ventilator care bundles is currently recommended
as best practice in reducing the incidence of VAP
(Lawrence and Fulbrook, 2011). Elevation of the head
of the bed of between 30 and 45 is also recommended
(How-to Guide, 2012) as part of such bundles. The
semirecumbent position may be associated with a
decreased incidence of VAP (Muscedere et al., 2008).
While antiseptic oral decontamination is inexpensive
and relatively safe, it may yet have a role in reducing
the incidence of VAP but that role has yet to be
fully evaluated. There is concern that given time and
antimicrobial use, resistance will inevitably emerge
(Dallas and Kollef, 2009). It is likely that chlorhexidine
may simply delay the development of VAP rather than
prevent it and may explain its greater effectiveness
in cardiothoracic patients (Dallas and Kollef, 2009). A
multi-faceted approach is essential.

CONCLUSION
VAP continues to be a leading cause of mortality and
morbidity in patients hospitalized in the ICU. It is also
linked to increased length of stay and consequently
increased costs. Ventilator care bundles have been
developed in an attempt to reduce the incidence
of VAP. Central to such an initiative is mechanical
hygiene and oral decontamination.
Patients are admitted to the ICU with oral hygiene
issues such as bacteria growing on dental plaque
contributing to the development of VAP. Mechanical
hygiene is an attempt to remove plaque. There
is some evidence that tooth brushing is effective
at removing plaque and that electric toothbrushes
are more effective compared to standard oral care.
However, the frequency of such an intervention and
the use or not of toothpaste has not been established.
There is some evidence supporting the use of
chlorhexidine in reducing the incidence of VAP but
this effect is strongest in cardiosurgical patients. If oral
decontamination is to be incorporated into ventilator
care bundles current research suggests that a 2%
concentration is more effective compared to lesser
concentrations.
Current studies suffer from a number of methodological issues that make it difficult to evaluate the

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Oral hygiene preventative strategies

efficacy of mechanical hygiene and oral decontamination. These include heterogeneous populations, inconsistency in the definition of VAP, small sample sizes
and patients receiving multi-faceted interventions.
Future research investigating the efficacy of mechanical

hygiene and oral decontamination should consistently

define VAP, include a more homogenous population
and control for such variables as bed elevation and
sub-glottic drainage since it is difficult to come to
conclusions when more than one intervention is made.

WHAT IS KNOWN ABOUT THIS TOPIC

Ventilator-associated pneumonia is associated with increased mortality, increased stay in intensive care and prolonged hospital stay.
Plaque formation and the loading of plaque by bacteria is increased in critically ill patients.
The incidence of nosocomial pneumonia through the removal of dental plaque may be reduced by improving oral hygiene.
WHAT THIS PAPER ADDS

In relation to mechanical removal, patients receive other VAP protective strategies which may confound results.
Chlorhexidine in concentrations of 2% seem to be more effective.
Mechanical hygiene and oral decontamination strategies are less effective in patients with comorbidities.
Methodological issues make it difficult to evaluate the efficacy of mechanical hygiene and oral decontamination strategies.

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