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Journal of Infection Prevention 2015, Vol. 16(2) 76 –81 DOI: 10.1177/1757177414560252 © The Author(s) 2014 Reprints and permissions: sagepub.co.uk/journalsPermissions.nav jip.sagepub.com
Journal of Infection Prevention
Introduction
Ventilator associated pneumonia (VAP) is pneumonia that appears in an intubated patient 48 or more hours from the onset of ventilation or up to one week after ventilation is discontinued (American Thoracic Society and Infectious Diseases Society of America, 2005; Fields, 2008). The signs and symptoms of VAP are similar to those of other pneumonias and include the following:
1. A change in body temperature to above 38 degrees C or below 36 degrees C
2. The appearance of new infiltrate on chest x-ray 3. A white blood cell count of less than 4,000 or greater
than 12,000
4. The appearance of or change in phlegm (purulence) (American Thoracic Society and Infectious Diseases Society of America, 2005).
Mouth-related risk factors for VAP include the forma- tion of bacterial colonies in the mouth, the accumulation of pathogenic bacteria on the surface of the teeth,
The effect of different oral hygiene treatments on the occurrence of ventilator associated pneumonia (VAP) in ventilated patients
Amiram Lev, Abu Sebeih Aied and Shibli Arshed
Abstract
Background: We compared the incidence of ventilator associated pneumonia (VAP) among patients treated with comprehensive oral care to those treated with conventional methods of oral care.
Methods: We conducted a prospective, controlled study in an intensive care unit of 90 ventilated patients. Patients in the study group received a comprehensive oral hygiene treatment regimen that involved tooth brushing, suctioning, sodium bicarbonate, rinsing with an antiseptic solution containing 1.5% hydrogen peroxide and a mouth moisturiser. Patients in the control group received a more conventional treatment that included cleaning with a sponge and atraumatic clamp, and rinsing with a 0.2% solution of chlorhexidine gluconate.
Results: Among the 90 patients admitted to the ICU, 8.9% of the study group developed VAP compared with 33.3% of the control group (p< 0.004). The development of VAP per 1,000 ventilation days was 10.2 in the study group, and 29.5 in the control group (p< 0.06). The mean number of ventilation days and the mean number of hospitalisation days were also lower in the study group.
Conclusions: In patients who are ventilated, a comprehensive oral hygiene treatment regimen that includes tooth brushing, suctioning and rinsing with an antiseptic is more effective in preventing VAP than more conventional protocols.
Keywords Chlorhexidine gluconate, comprehensive oral hygiene, nosocomial infection, tooth brushing, VAP, ventilator associated pneumonia
Date received: 19 May 2014; accepted: 19 October 2014
General Intensive Care Unit, Emek Medical Center, Israel
Corresponding author: Amiram Lev, General Intensive Care Unit, Emek Medical Center, Afula 18101, Israel. Email: icuadm1@clalit.org.il
560252 BJI0010.1177/1757177414560252Journal of Infection PreventionLev et al. research-article2014
Original Article
Lev et al. 77
development of plaque, and aspiration of secretions from the oral cavity (Rello et al, 2002; Schleder, 2003). Studies have shown that, within 24 hours of admission to an inten- sive care unit (ICU), patients can become colonised with pathogenic bacteria such as Pseudomonas, Acinetobacter, and methicillin-resistant Staphylococcus aureus (MRSA) (Sole et al, 2002; El-Solh et al, 2004; Garcia et al, 2004; Rello, 2005; Fields, 2008).
Among mechanically ventilated patients, VAP is the most common nosocomial infection (Luyt et al, 2005). The reported incidence of VAP varies because of overlap with other lower respiratory infections, surveillance strategy, case definition, and diagnostic procedures. In its High Impact Intervention guideline, the United Kingdom Department of Health mentions that VAP is the most fre- quently occurring infection in patients having been admit- ted to the ICU (Vincent et al, 2006; United Kingdom Department of Health, 2011). This National Health Service (NHS) guideline also says that, in addition to an increased mortality rate associated with VAP (Melson et al, 2009; United Kingdom Department of Health, 2011), this noso- comial pneumonia is associated with increased duration of ventilation, ICU and total hospital length of stay, and healthcare expenses (Safdar et al, 2005; United Kingdom Department of Health, 2011). Preventing this type of infec- tion, therefore, is feasible using cost-effective bundles.
Efforts to describe the global burden of VAP reflect the challenge of gathering reliable data. It is accepted that VAP is associated with prolonged periods of mechanical ventila- tion, extended hospitalisations, and excessive use of anti- microbial medications (Fischer et al, 2000; Coffin et al, 2008; Edwards et al, 2009; Bekaert et al, 2011; O’Grady et al, 2012). In terms of financial implications, VAP has been shown to cost an additional US$29,000 to $40,000 per patient (Rello et al, 2002; Schleder, 2003; Fields, 2008; Restrepo et al, 2010). Moreover, VAP is associated with higher mortality. Although some controversy surrounds the determination of mortality rates attributable to VAP (Edwards et al, 2009; Bekaert et al, 2011; O’Grady et al, 2012), the VAP mortality rate has been reported to be as high as 40% to 80% (Fagon et al, 1993; Porzecanski and Bowton, 2006; Fields, 2008).
The results of recent quality improvement studies show that proper oral care lowers the rate of VAP in acute care facilities (Coffin et al, 2008). Using an oral care protocol reduced the VAP rate from 12 to 8 per 1,000 ventilator days (p = 0.06) and also significantly reduced duration of venti- lation, length of stay, and mortality (Garcia et al, 2009).
As oral care continues to emerge as an issue that can change the prognosis of critically ill patients, conventional methods of oral hygiene are frequently evaluated for their efficacy in reducing VAP. Evidence has shown that pre- venting bacterial colonisation of the oropharynx prevents the development of VAP. Several studies have proven that the removal of dental plaque is a key to removing bacteria
from the oropharynx, and the most effective way to remove the plaque is through tooth brushing and suctioning simul- taneously. Others have found that tooth brushing removes plaque more effectively than the use of soft swabs or gauze (Pearson and Hutton, 2002; Schleder, 2003; Binkley et al, 2004; El-Sohl et al, 2004; Shinn, 2004; Fields, 2008; Heo et al, 2008).
We conducted a study to examine the effects of an oral hygiene treatment that includes tooth brushing, cleaning of the oral cavity, and rinsing with antiseptic. We wished to compare the incidence of VAP among patients treated with oral care combined with the brushing of teeth to those treated with conventional methods of oral care. We hypoth- esized that a correlation would be found between the type of oral hygiene treatment administered and the VAP inci- dence in ventilated patients in the ICU.
Methods
We conducted a prospective, controlled study in the hospi- tal ICU. The ICU is a general intensive care unit that admits patients from all hospital departments, including trauma, surgery, severe infection and internal medicine patients. Our study population included all ventilated patients in the ICU between August 2007 and October 2009. Upon admis- sion to the ICU, patients were alternately allocated to either the study group (n=45) or the control group (n=45). We excluded from our study patients who were younger than 18 years, patients with a clinical diagnosis of pneumonia at the time of intubation, immunosuppressed patients, preg- nant women, and burn patients.
All patients admitted to the general intensive care unit (GICU) were allocated to either the study or control group, aside from those filling the exclusion criteria stated above. Each patient was allocated only on the basis of the time entering the GICU. Patient surveillance was performed by an independent person (infectious disease nurse) who was una- ware of the patient allocation group. National Healthcare Safety Network (NHSN) criteria were used to diagnose VAP.
The study was approved by the hospital local ethics committee and written informed consent was signed by each patient or his/her legal guardian.
Data collection
Data collection included the following factors:
•• The number of days in the ICU •• The number of days of hospitalisation •• The number of days of ventilation •• The use and type of antibiotics •• Mortality within 30 days of study enrolment •• Development of VAP according to definition
(American Thoracic Society and Infectious Diseases Society of America, 2005).
78 Journal of Infection Prevention 16(2)
Oral care
The oral care protocol of the study group was implemented three times per day with the use of the Q-Care Suction Oral System from Sage Products LLC (Toothette® Oral Care Suction Toothbrush with Alcohol-Free Mouthwash and Mouth Moisturizer) (Sage Products LLC; Cary, IL). Each patient assigned to this group underwent a daily assessment of the oral cavity (lips, tongue, oral mucosa, gums, and teeth) and sputum. A member of the treatment team completed a structured form, which included details such as body tem- perature, chest x-ray findings, leucocyte count, Acute Physiology and Chronic Health Evaluation (APACHE) II score, ventilation mode, and culture results. The teeth were then brushed and oral discharge removed with a soft-bristle suction toothbrush, and suction swab. Sodium bicarbonate was used on the suction toothbrush to mechanically clean, refresh, and deodorize the oral cavity. In many ICUs in Europe, regular toothbrushes are often used in conjunction with suctioning through a soft or hard catheter. We find, however, that a small-headed toothbrush that incorporates suctioning offers greater comfort, ease of control, and effi- cacy. The oral cavity was cleaned with Sage Perox-A-Mint (1.5% hydrogen peroxide) solution. Finally, the oral cavity and lips were moistened with 2 grams of Toothette® Oral Care Mouth Moisturiser, a water-based moisturiser contain- ing vitamin E to promote the healing of lesions.
For the control group, oral care was also carried out three times per day. Each patient in this group underwent assessment of oral cavity and sputum with the use of the same structured form. Oral treatment was then adminis- tered using the conventional protocol as follows: Thorough cleaning of the oral cavity with a sponge and atraumatic clamp was completed, followed by spreading throughout the oral cavity of Tarodent, which contains a 0.2% solution of chlorhexidine gluconate.
Antibiotic use
Antibiotics were used to treat both the study group and the control group. The antibiotics were divided into three
groups. The first-line antibiotics included cephalosporins, quinolones, and macrolides. The second-line antibiotics included piperacillin-tazobactam. The third-line antibiotics included vancomycin, carbapenems, and anti-fungal and anti-viral drugs. Combinations of antibiotics were also used.
We use the first-line antibiotics for infections acquired outside of the hospital. The second line is used for hospital- acquired infections or for non-responders to first-line antibiotics. The third line is reserved for hospital-acquired infections or bacteria not sensitive to the first- or second- line antibiotics, or for outbreaks of viral infections, such as influenza.
Patient characteristics
Characteristics of the study population were summarized through descriptive statistics (Table 1). In the study group, 55.5% of the patients were male. The age range was 21 to 93 years; mean age was 68.7 years (SD, 15.6). In the con- trol group, 53.3% of the patients were male. The age range was 27 to 88 years; mean age was 71.8 (SD, 14.8). Demographic characteristics did not differ significantly between the study and control groups (p> 0.34).
There were no statistically substantial differences in pri- mary diagnosis between the two groups (p>0.65) (Table 2). The largest differences, however, occurred with regard to patients with cardiovascular disease (22.2% in the study group; 33.3% in the control group (p=0.239)), and patients who had undergone surgery/trauma (33.3% in the study group; 24.4% in the control group (p=0.352)). The mean APACHE II score was 19.1 (SD, 3.2) in the study group, and 18.2 (SD, 3.5) in the control group (p= 0.73) (Table 2). Patient baseline characteristics were similar across groups, providing a good baseline for comparison.
The diagnosis of VAP was based upon NHSN criteria. An independent person reviewed the data and decided whether the diagnosis of VAP could be made. This person was unaware of the group allocation of the patient. Statistical analyses were performed by the hospital statistician.
Statistical analysis
The data were analyzed using SAS® 9.2 software. Categorical variables were compared using the chi-square test and Fisher exact test. Comparisons of matched subjects with respect to the number of days of first-, second-, and third-line antibiotic use were performed using the Wilcoxon rank-sum test. A p value < 0.05 was considered statistically significant.
Results
During the study period, among the 90 patients admitted to the ICU, 8.9% of the study group developed VAP compared
Table 1. Patient characteristics.
Study group Control group
Number of patients
45 45
Sex Male: 25 (55.5%) Male: 24 (53.3%)
Female: 20 (44.4%) Female: 21 (46.6%)
Age (years) Range: 21–93 Range: 27–88
68.7 ± 15.6 71.8 ± 14.8
There were no statistically significant differences in demographic charac- teristics between the two groups (p >0.34).
Lev et al. 79
with 33.3% of patients in the control group (p< 0.004). The development of VAP per 1,000 ventilation days was 10.2 in the study group, and 29.5 in the control group (p< 0.06) (Table 3).
Hospital mortality did not differ significantly between the study and control groups (26.7% vs. 28.9%, respec- tively (p< 0.46). However, patients in the study group spent a mean of 11.09 days in the ICU; those in the control group spent 14.98 days (p< 0.151). The mean number of days on a ventilator was 8.39 in the study group vs. 12.69 in the control group (p< 0.044). The mean number of days of hospitalisation was 25.38 in the study group, and 31.71 in the control group (p< 0.02). The study group patients had a mean of 7.2 treatment days with antibiotics compared with 9.7 in the control group (p< 0.413). The study group had a mean of 5.76 treatment days with first-line antibiotics compared with 8.97 in the control group (p = 0.0267), 5.58 treatment days with second-line antibiotics compared with 7.42 in the control group (p = 0.1820), and 7.93 treatment days with third-line antibiotics compared with 9.92 in the control group (p = 0.2255).
Discussion
Dental plaque and other components of the oral cavity serve as perfect breeding grounds for pathogenic bacteria (Garcia et al, 2004; Fields, 2008). In patients who are ven- tilated, a comprehensive oral hygiene treatment regimen that involves tooth brushing, suctioning, rinsing with an antiseptic, and moisturising is more effective in preventing VAP than more conventional protocols.
Fields (2008) conducted a randomised, controlled trial in a 24-bed ICU with stroke patients randomised to usual VAP prevention measures plus timed tooth brushing vs. the usual VAP prevention measures. This study demonstrated
that a regimen including comprehensive oral care decreased the occurrence of VAP. The VAP rate dropped to zero within one week of beginning the every-eight-hours suction tooth- brushing regimen in the intervention group. The study was amended after six months, dropping the control group, because VAP rates decreased so dramatically. From then on, all intubated patients’ teeth were brushed every eight hours, maintaining a zero rate until the study was com- pleted (Fields, 2008).
These and other studies have prompted various govern- ment and medical organisations to include comprehensive oral care as part of their guidelines for preventing VAP. The American Association of Critical-Care Nurses (AACN), the Institute for Healthcare Improvement (IHI), the Centers for Disease Control and Prevention (CDC), and the International Nosocomial Infection Control Consortium (INICC) refer to the importance of including daily and comprehensive oral care in controlling pneumonia (Tablan et al, 2004; Al-Tawfiq and Abed, 2010; Lynn-McHale Wiegand, 2011; Rosenthal et al, 2012).
While the overall patient characteristics in our study did not differ significantly, the study group contained propor- tionately more surgery/trauma patients than the control group (33.3% vs. 24.4%, p = 0.352), as well as more infected patients (17.8% vs. 11.1%, p = 0.368) and fewer patients with cardiovascular disease (22.2% vs. 33.3%, p = 0.239). These patient characteristics demonstrate that the patients were well matched for their primary diagnosis, yet it appears that the study group contained proportion- ately more high-risk patients. Thus, our results are not confounded by underlying disease state.
The oral care regimen administered to our study group included use of an antiseptic containing 1.5% hydrogen peroxide compared with that of the control group, which contained 0.2% chlorhexidine gluconate. Our intent is not
Table 2. Primary diagnosis and mean APACHE II score.
Study group Control group p-value
Primary diagnosis*:
• Cardiovascular disease 22.2% 33.3% 0.239
• Surgery/trauma 33.3% 24.4% 0.352
APACHE II (Mean ± SD) 19.1 ± 3.2 18.2 ± 3.5 0.73
*There were no statistically substantial differences in diagnosis between the two groups (p>0.65).
Table 3. Development of ventilator associated pneumonia (VAP).
Study group Control group p value
Percentage of patients that developed VAP 8.9 33.3 < 0.004
Development of VAP per 1,000 ventilation days 10.2 29.5 < 0.06
80 Journal of Infection Prevention 16(2)
to press any antiseptic preference. We actually believe that chlorhexidine gluconate is a potent and very effective oral antiseptic and probably our top choice for a VAP prevention protocol as also was endorsed by the British Association of Critical Care Nurses (BACCN), though at lower concentra- tions such as 0.12% in order to avoid chlorhexidine gluco- nate potential side effects. Our approach indeed aims to highlight that a good antiseptic needs to be part of an inte- grated and comprehensive oral care protocol.
Furthermore, the efficacy of any oral antiseptic could be compromised if dental plaque is not consistently removed, underscoring the importance of tooth brushing.
In the United Kingdom, controlling VAP presents a chal- lenge similar to that of other European countries. Data pub- lished by the European Centre for Disease Prevention and Control (ECDC) based on National Health Service trusts’ reporting show a mean VAP rate of 13.5 per 1,000 ventilator days in ICU patients (European Centre for Disease Prevention and Control, 2011). Additionally, in its latest annual epidemio- logical report, which was published in December 2013, the ECDC identifies Klebsiella spp., MRSA, Escherichia coli, and Enterobacter spp. as some of the most common pathogens causing ICU-acquired pneumonia in the United Kingdom (European Centre for Disease Prevention and Control, 2013).
To address these issues, the Critical Care Manual of Clinical Procedures and Competencies, endorsed by the BACCN and published in 2013, mentions key components that should be included in oral care protocols to prevent pneumonias:
•• Tooth brushing (at least twice a day) •• Completely removing toothpaste from the oral cav-
ity to prevent it from drying there •• Using an antiseptic solution (in this manual, 0.12%
chlorhexidine gluconate) •• Implementing a small-headed toothbrush that allows
for better manoeuvering inside the mouth of the intubated patient (Mallett et al, 2013)
The research performed in our facility sought to address the same types of VAP-related challenges facing British and European acute care facilities, and demonstrated in a statis- tically successful manner that these components are indeed important elements in any bundle targeting the control of pneumonia-associated pathogens.
We know that hospital costs increase substantially with additional ventilation and hospitalisation days. Acquired pneumonia in ventilated patients contributes to the eco- nomic burden because of the need for more ventilation and hospitalisation days. We found a statistically significant reduction in the mean number of ventilation days and in the mean number of hospitalisation days between the study and control groups. Although our study did not show a differ- ence in mortality rates between the study and control groups, a reduction in the factors contributing to economic
burden is enough to justify promotion of an oral hygiene treatment regimen that is comprehensive and proven to reduce VAP rate in ICU patients.
Study limitations
We conducted a prospective, controlled study that was unblinded. Patients were alternately allocated to either the study or control group. The unblinded nature of the study has the potential to introduce bias. Patients received vary- ing antibiotic regimens, which could have affected VAP rates. Finally, providers of oral care could have varying skill in the application of the protocol, introducing the pos- sibility of operator bias.
Recommendations
We propose the following recommendations with regard to oral hygiene treatments in ventilated patients:
1. The continued tracking of the development of VAP in ICU patients
2. Ongoing awareness of VAP prevention through con- tinued education of the team – emphasizing the importance of timely and proper mouth cleaning
3. Inclusion of suction tooth brushing two to three times a day as part of the oral hygiene protocol of the ICU
4. A continuation of the discussion of additional ways to reduce VAP in ventilated patients
5. A standardization of oral hygiene treatment proto- cols among ICU medical teams
6. Implementation of oral hygiene treatment protocols in other hospital facilities treating ventilated patients.
Acknowledgements
The authors would like to thank Nava Teitler, Infection Control Coordinator, Emek Medical Center, Afula, Israel; and Susan J. Antonini Affinito, for assisting with the writing of this manuscript.
Declaration of conflicting interest
On behalf of all authors, the corresponding author states that there is no conflict of interest.
Funding
Sage Products LLC provided funding to support the preparation of this manuscript.
Peer review statement
Not commissioned, blind peer-reviewed.
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