Ventilator-associated pneumonia (VAP) is the most common cause of nosocomial infection in the intensive care setting and is responsible for increased length of treatment with mechanical ventilation, hospital length of stay, and mortality rate.1-4 Many factors influence the incidence of VAP in critically ill patients. In response to the need to reduce the incidence of VAP, the Centers for Disease Control and Prevention5 developed a VAP bundle, which consisted of elevation of the head of the bed to 30[degrees] to 45[degrees], standard infection-control precautions, management of respiratory equipment, prevention of aspiration, oral hygiene, and education of staff.6

The incidence of VAP in Australian intensive care units (ICUs) has been estimated at 6.2 per 1000 days of treatment with mechanical ventilation.2 In the United States, VAP costs the health care system $2 billion per year, with a single incidence of VAP costing approximately $30 000 to $40 000.7,8 Currently, the Centers for Disease Control and Prevention recommend that an oral care program be implemented to help reduce the risk of VAP.5

Effective oral hygiene has been linked to a decreased incidence of VAP.6,9-11 Currently, minimal literature is available related to best practice for oral hygiene in patients being treated with mechanical ventilation. Despite many recent reviews related to VAP,12-16 no reviews address the specific clinical issue of infection control with oral hygiene or emphasize a preventative nonantibiotic approach to reduce the incidence of VAP. The World Health Organization advocated on World Health Day 2011 for the rational use of antibiotics, as a result of increasing microbial resistance, thus emphasizing the need for prioritizing infection control in clinical practice, rather than antibiotic administration. This recommendation includes best practice oral hygiene in the prevention of VAP.17

Pneumonia is caused by infiltration of microbial agents in the lung parenchyma, causing inflammation.18Ventilator-associated pneumonia is defined as pneumonia that occurs 48 hours or more after intubation.2 Colonization of dental plaque by gram-negative bacteria is an important contributor to the oropharyngeal bacterial pool in patients who are sedated and patients who are being treated with mechanical ventilation.19 This type of colonization has been attributed to a reduction of salivary flow, infrequent swallowing, and lack of natural movements of the tongue and mouth.19 In addition, failure to clean the oral cavity and oropharynx and brush the teeth results in biofilm, dental plaque formation, and the increased colonization and growth of pathogenic organisms.11,19-25

Treatment with mechanical ventilation is lifesaving. However, when the epiglottis is bypassed by an endotracheal tube, the body's natural defense mechanism against descending pathogens entering into the respiratory tract from the oropharynx is impaired,2 which makes patients receiving ventilator support more susceptible to nosocomial airway infections. Oral hygiene has been identified as one important weapon in the defense against VAP.6,10

Intubated patients are at 6 to 21 times higher risk of VAP than patients who are ventilated noninvasively.2,3 In many cases, more than 1 pathogen causes the pneumonia.1,3,19 The risk of VAP also increases 1% to 3% every day that the patient receives treatment with mechanical ventilation.1,3 Because of the critical nature of intensive care patients, they are frequently immunocompromised and thus are at more risk of infections.2,4

As VAP can affect 10% to 48% of all patients being treated with mechanical ventilation, an understanding of the factors that contribute to its prevention is essential.1 These factors include patient positioning, endotracheal suctioning, sedation management, and peptic ulcer prophylaxis, and these factors should be considered in conjunction with oral care.6,26-29 However, for the purpose of this literature review, we focus on oral hygiene practices and its contribution to VAP.

Clinicians need to review nursing practices around oral care, including oral care product selection, method of application, and compliance with oral care protocols.2,3,7 Compliance with some of the preventative techniques to help reduce VAP rates has been reported as being low in some ICUs.1,24,30,31 Ross and Crumpler32 identified that oral care has been poorly understood by some nurses and was seen as a "comfort measure" and not as a method of preventing VAP. They surmised that this lack of understanding was responsible for poor compliance by nursing staff to oral hygiene protocols.32,33

Methods

A systematic review of the literature was conducted. This type of review is considered particularly useful for cause-and-effect analysis of literature and is considered to minimize the potential for bias.34

Sample

The literature review guidelines used to critique the chosen articles were taken from Schneider, Letts et al, and Law et al.34-37 These guidelines for critical review of literature were chosen as they were developed and tested by university scholars and deemed to be the most appropriate tools for this review.

Using the NHMRC, the Australian national research levels of evidence hierarchy, the classification of research in the chosen articles was evaluated.38 The hierarchy of evidence was developed by the Australian NHMRC to assist researchers in categorizing the type and quality of the research for analysis.38 All studies were analyzed for their strengths and weaknesses and graded against the NHMRC evidence hierarchy38 (see Table 1).

Table 1-a: Reviewed Articles

Findings

Results from the studies were difficult to compare, as the research methodologies, interventions administered, and protocols analyzed were different in each study. Studies generally implemented multiple interventions such as applying a revised or new oral care protocol, following the ventilator bundle,39 implementing an education program and performing oral care, and using a specific product and application method. The use of various interventions made isolating the effects of individual interventions difficult to assess.

The 4 main themes identified (Table 2) from the analysis of the literature were as follows:

Table 2: Oral Care Themes of Selected Research Studies

Findings from each of these themes are discussed in the sections that follow.

Oral Care Protocols

Numerous studies created new assessment and oral hygiene protocols to reduce the incidence of VAP.11,21,23,25,32,33,40-43 In other studies, existing oral care protocols were adapted to reduce high levels of VAP. The clinicians in the study changed documentation, assessments, and methods of oral care.25,32,44-46 Several studies observed current protocols to understand the practices surrounding oral health in Malaysia, the United States, and England.33,47,48 Having a protocol in place was reported to increase the quality of oral hygiene and decrease VAP rates. However, many studies did not outline the content of their oral hygiene protocols.11,21,23,32,42,43,45,46,49-55

In several studies, a multidisciplinary protocol was created that prescribed the frequency and method of oral care to reduce the incidence of VAP.42,49,56 To increase compliance, Cutler and Davis49 implemented a 24-hour oral care kit instituted at the bedside, with ongoing assessment and training of oral care practices provided; they found that without oral care protocols, oral care was undertaken infrequently, and important steps were omitted.49

A national survey by Kearns et al51 researched current oral care practices in 24 Scottish ICUs. Eighty-eight percent of the ICUs undertook oral care assessments, but only 29% had current oral care protocols, indicating a lack of protocol-based oral care.51 Similarly, Soh et al47 undertook a survey of Malaysian hospitals to determine the oral care practices within Malaysian ICUs and the nurses' attitudes toward oral hygiene. Although nurses had a positive attitude toward oral care, there was little consensus on oral hygiene practices, and the nurses did not adhere to evidence-based practice because they did not use toothbrushes.

Oral Care Product and Application

Products used for oral care varied and included petroleum jelly, sodium chloride, povidone-iodine, and chlorhexidine, with chlorhexidine being the product of choice to reduce VAP in patients being treated with mechanical ventilation (Table 2).9,20,22,23,25,40,43,44,46,50,52,53,55

Various methods are available to perform oral hygiene, with very little consensus among oral hygiene protocols.9,20 DeRiso et al11 used a 0.12% chlorhexidine oral rinse in their original study on oral hygiene, with an improvement in their VAP rates. Hutchins et al50 used 0.12% chlorhexidine, applied with a suction toothbrush every 4 hours, and cleansed the oral cavity with hydrogen peroxide-soaked suction swabs. An immediate improvement was reported in oral hygiene practices on implementation of the protocol, with VAP rates decreasing by 89% over 3 years.50

Munro et al53 compared 4 oral care application methods and products. One group received an oral swab soaked with 0.12% chlorhexidine twice a day, another used a toothbrush alone 3 times a day, the third group had a combination of tooth brushing 3 times a day and chlorhexidine swabs every 12 hours, and the control group received the established unspecified, oral care practice of the studied unit. The use of chlorhexidine swabbing reduced VAP, but the study articulated that using a toothbrush and chlorhexidine was no more beneficial than chlorhexidine swabbing alone.53

Pobo et al46 compared standard oral care with standard care with the addition of an electric toothbrush. Standard care included oral cavity suctioning, gauze soaked in 0.12% chlorhexidine applied to oral cavity surfaces with 0.12% chlorhexidine injected into the mouth and aspirated after 30 seconds every 8 hours. Similar to Munro et al,53 Pobo et al46 found that electric tooth brushing in addition to standard care did not significantly affect VAP rates and did not affect the inception of VAP. The study was discontinued as a result of a lack of statistically significant results.46

Sona et al43 implemented a protocol of brushing with 0.7% sodium monoflurophosphate paste onto the patient's teeth, rinsing with water, and suctioning every 12 hours. A foam sponge was used to apply 0.12% chlorhexidine, and the incidence of VAP was reduced.43

Grap et al44 used one 5 mL dose of 0.12% chlorhexidine to all areas of the oral cavity for their intervention. The control group received standard oral care but did not receive chlorhexidine. These authors found that the single dose of chlorhexidine reduced the incidence of VAP; VAP developed in 55% of control patients by 48 to 72 hours, compared with 33.3% in the intervention group.44

Genuit et al25 added 0.12% chlorhexidine to their weaning protocol and found an immediate reduction and delay in the incidence of VAP.

Berry et al40 studied 3 different groups. The control group received oral care with water every 2 hours.40 The second group received sodium bicarbonate every 2 hours, and the last group had twice-daily irrigations with 0.2% chlorhexidine oral rinse and irrigations with sterile water every 2 hours.40 No difference was found between the intervention groups, with a VAP rate of 5%; however, the control group had a VAP rate of 1%.40

Fourrier et al22,23 found that decontamination with 0.2% chlorhexidine 3 times a day reduces oral contamination and therefore may reduce the incidence of VAP. However, the later study showed that this protocol was insufficient to reduce the incidence of respiratory tract infections with multiresistant bacteria.23

Koeman et al52 compared 3 different oral care groups. The treatments in the 3 groups included 2% chlorhexidine in petroleum jelly, 2% chlorhexidine, and 2% colistin in petroleum jelly, and the placebo group received only petroleum jelly. All gels were applied digitally every 6 hours.52 The combination of chlorhexidine and colistin significantly reduced both gram-positive and gram-negative microorganisms, whereas chlorhexidine alone mainly affected gram-positive microorganisms.52

Tantipong et al55 studied a protocol that included oral suctioning, brushing the teeth, and rubbing 2% chlorhexidine on the oropharyngeal mucosa 4 times a day. The control group received the same care but used saline rather than chlorhexidine.55 Chlorhexidine was superior to sodium chloride in reducing VAP.55

Mori et al42 used a completely different product. The control group received no oral care, and the intervention group received oral care using 20-fold diluted povidone-iodine swabs, brushing with weakly acidic water, and repeated swabbing with povidone-iodine every 8 hours.42 Ventilator-associated pneumonia rates dropped significantly when oral care was provided.42

No agreement was found among these studies on oral hygiene practices. The method of oral care application and product selection were not consistent.9,20,43,50,52,53 However, chlorhexidine was considered the cleansing solution of choice.9 Inconsistency was reported in the frequency of oral care recommended, and inconclusive information was available on the effect of tooth brushing, whether it be manual or electric, on VAP rates.42,43,50,52,53

Assessment of Nurses' Oral Hygiene Practices

The importance of assessing nursing oral hygiene practices was highlighted, as oral care protocols were not sufficient alone to reduce VAP rates.32,43 Nurses were observed while performing oral care on patients being treated with mechanical ventilation and received direct feedback on their performance after completing the task.32 Compliance with oral hygiene regimens was augmented when accompanied with this recurrent assessment of nursing practice. Assessment, in conjunction with education, was found to continuously raise the profile of the importance of oral hygiene in regard to reducing VAP (46% reduction in VAP rates). Sona et al43 documented a 100% compliance rate when nurses were being assessed and audited.

Two studies discussed the significance of testing the competency of nursing staff after education had taken place.45,50 Assessment of the nurses' knowledge of the implemented protocol improved the compliance of oral care by 80%, which in turn decreased the VAP rates by 33%.45

Staff members participating in the study by Sona et al43 were required to undertake annual oral care competency tasks, and all new staff employed had to receive oral care education, which maintained compliance with oral hygiene protocols and maintained the reduction in the incidence of VAP.

Nurse Education and Training

Numerous studies discussed the importance of education for nurses in reducing VAP rates.21,23,24,30,31,40,45,48-50,52 A multifaceted approach to education was found to enhance learning, including visual posters, pictorials, education sessions, in-service training, and encouragement of self-learning.32,40,43,45

Education reinforced the oral hygiene protocols, products required, and the physiological knowledge behind oral hygiene. Through evidence-based education programs, Ross and Crumpler32 supported the perception that oral care was essential in preventing VAP, which reinforced the importance of oral hygiene as a powerful tool against VAP and not just a comfort measure.21,24,32,40,46,52

Keeping educators constant ensured that consistent education was provided to all nurses. After comparing results from the preeducation phase where no oral care was undertaken with those from the posteducation phase, Cutler and Davis49 found that all aspects of oral care increased after the education intervention. With regular education and guidance, oral care remained consistent.32,42

Despite the implementation of a creative, structured education program, Bingham et al30 found that their compliance with mouth care protocols did not improve. The failure to achieve compliance may have been influenced by a complicated, time-intensive protocol, in a time-challenged environment, with a high turnover of nursing staff, supervisors, and leadership, making sustained change difficult.30

Hutchins et al50 was the only study that reeducated their nurses a year after the original education intervention, when VAP rates were seen to be on the increase again. This reeducation improved the method of providing oral care to patients and again decreased the VAP rates.50

Despite the introduction of oral hygiene education, many nurses believed that they required further training to improve oral care practices. These studies highlighted that most training and education nurses received in oral care were not formal, but through on-the-job training.31,51,54

Discussion

Preventing VAP through oral care is essential to avoid the development and spread of antibiotic and multidrug-resistant pathogens.1,10,17,57 Research has highlighted that oral care is an important intervention in the reduction of VAP.27,50,52,55 Implementation of oral care protocols and/or education programs has demonstrated positive impact on VAP rates.30,31,33,44,45,49-51 No consensus was found among studies on oral hygiene practices and protocols. The most popular oral care product used throughout the selected articles was chlorhexidine, specifically 0.12%.43,46,50,53 However, several researchers recommended researching the effects of a stronger concentration of chlorhexidine.43,46,50,53 Three studies tested 0.2% chlorhexidine, with conflicting results of its effectiveness in preventing VAP.22,23,40 Two studies used 2% chlorhexidine, and both found that this strength was safe and effective at preventing VAP.52,55 No research was uncovered that empirically determined which was the best concentration or product for oral hygiene; however, the meta-analysis of Labeau et al9 suggests 2% chlorhexidine.

Strengths and Limitations

To prevent performance bias, some of the studies did not inform nursing staff that a study was being performed, thus reducing the Hawthorne effect.32,46,55 Seven of the studies had large study groups, which assisted with internal validity.58,59 Nine of the twenty-six studies were conducted in more than 1 hospital setting, improving the generalizability.20,23,24,31,33,51-54

A limitation of the literature review was that only 26 studies were found to meet the inclusion criteria.60 Many patients included in the selected studies were removed from mechanical ventilation before the end of the study period,53 which did not allow the studies to measure long-term effects of oral care and VAP rates.53

The study by Pobo et al46 was discontinued half way through the study period, because of the lack of statistically significant results between study groups. The authors suggested that this might have been caused by the use of an endotracheal tube that was covered with a biofilm, which in itself is worthy of further investigation.46 Berry et al40 also prematurely terminated their study as a result of the discontinued production of one of their products.

This literature review included only studies that focused on adult intensive care patients, so results may not be generalizable to pediatric ICUs.61 Although all patients studied were in the intensive care setting, the diversity and acuity of patients varied between the studies, potentially altering results.45,52

Further Research and Implications for Practice

After reviewing the findings, some large gaps in the literature became apparent. The method of oral care product application was one of the main gaps discovered.27 Each of the studies used different combinations of application techniques, with no consistency or testing of the best method. Clinicians are recommended to address this gap in future research, as the potential exists to increase the effect oral care has on VAP rates.43,44,46,50,52,53,55 Further research testing the impact of varying concentrations of chlorhexidine is required.53

The use of a toothbrush was controversial, with some studies documenting it having an effect on VAP rates and others suggesting that it had no benefit over using chlorhexidine alone.9,43,46,47,50,53,55 The effect of both manual and electric tooth brushing on VAP rates needs to be explored further.50,53

Another inconsistency was the timing intervals for when oral care was provided. Future research should focus on the best timing intervals to prevent VAP. Many articles implemented more than 1 intervention at a time to prevent VAP, such as providing oral care, implementing an oral care protocol, and providing nursing education.30-33,40,46,48,53 It was difficult to identify the individual effects of each intervention. Future studies should separate these interventions and identify their individual effects.

The main recommendation for practice is the implementation of oral care assessment protocols to guide health care professionals about the best oral care product and application technique.56 Clinicians are recommended to implement an oral care protocol and education program in each intensive care setting.21,23,33,45,48-51

Regular reeducation of nursing staff in relation to oral care protocols, assessment, and application techniques is important in maintaining compliance with oral care standards.50,62 Bingham et al30 did not show an improvement in adherence to oral hygiene protocols after education. However, this failure was attributed to the rapid turnover of nursing staff, supervisors, and leadership, leading to a dilution of knowledge and therefore reduced compliance of staff to the new protocols.30 Education should address nurses' concerns that inhibit them from performing oral care, for example, potential dislodgement of the endotracheal tube, as this step should increase compliance.51 The protocol for oral care for patients being treated with mechanical ventilation contains some significant gaps in the literature, and further research is required to answer these issues.

Oral care is not the only intervention that has been studied to reduce the rate of VAP in patients being treated with mechanical ventilation. Other methods, such as patient positioning and ventilator bundles, should also be researched and used in conjunction with oral care to best prevent VAP.26-28,41

Conclusion

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