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ORAL HEALTH STATUS AND DEVELOPMENT OF VENTILATOR-

ASSOCIATED PNEUMONIA: A DESCRIPTIVE STUDY


By Cindy L. Munro, RN, PhD, ANP, Mary Jo Grap, RN, PhD, ACNP, R.K. Elswick, Jr, PhD, Jessica McKinney, BS,
Curtis N. Sessler, MD, and Russell S. Hummel III, BS, MS. From Adult Health Department, School of Nursing
(CLM, MJG, RKE), Department of Biostatistics (RKE, JM), Division of Pulmonary and Critical Care Medicine,
Department of Internal Medicine (CNS), and Department of Surgery (RSH), School of Medicine, Virginia
Commonwealth University, Richmond, Va.

• BACKGROUND Ventilator-associated pneumonia is a significant cause of morbidity and mortality and


may be influenced by oral health.
• OBJECTIVE To describe the relationship between ventilator-associated pneumonia and oral health status,
changes in oral health status during the first 7 days after intubation, and microbial colonization of the
oropharynx and trachea.
• METHODS A total of 66 patients were enrolled within 24 hours of intubation and were followed up for
up to 7 days. Data on oral health measures and the Clinical Pulmonary Infection Score (CPIS) were col-
lected at baseline, day 4 (n = 37), and day 7 (n = 21). A regression model was used to predict risk of
pneumonia at day 4.
• RESULTS Dental plaque and oral organisms increased over time. Correlations were significant for
baseline and day 4 dental plaque (P < .001), baseline salivary lactoferrin and day 4 plaque (P = .01),
and lower salivary volume and higher day 4 CPIS (P = .02). Potential pathogens were identified in oral
cultures for 6 patients before or at the same time as the appearance of the organisms in tracheal aspi-
rates. Correlations were significant with day 4 CPIS for score on the Acute Physiology and Chronic
Health Evaluation (APACHE) II (P = .007), day 4 salivary volume (P = .02), interaction of APACHE II
score and day 1 CPIS (P < .001), and interaction of day 1 CPIS and plaque (P = .01).
• CONCLUSIONS Higher dental plaque scores confer greater risk for ventilator-associated pneumonia,
particularly for patients with greater severity of illness. Salivary volume and lactoferrin may affect the
risk. (American Journal of Critical Care. 2006;15:453-460)

V entilator-associated pneumonia (VAP) is


defined as pneumonia in a patient receiving
mechanical ventilation that was neither pre-
sent nor developing at the time of intubation. VAP
increases mortality,1 length of stay,2,3 and cost.2,4,5 Oral
health status can be compromised by critical illness
and by mechanical ventilation and is influenced by
nursing care.6,7 However, the extent of oral changes in
critically ill patients and the relationship between oral
health status and development of VAP have not been
extensively studied.
A major risk factor for VAP is colonization of
Corresponding author: Cindy L. Munro, RN, PhD, ANP, Professor, School of Nursing, the oropharynx by potential pathogens such as
Virginia Commonwealth University, Box 980567, Richmond, VA 23298-0567
(e-mail: cmunro@vcu.edu). Staphylococcus aureus, Streptococcus pneumoniae,
and gram-negative rods.8-11 Several factors contribute
To purchase electronic or print reprints, contact The InnoVision Group, 101
Columbia, Aliso Viejo, CA 92656. Phone, (800) 809-2273 or (949) 362-2050 to the importance of oral health status in the develop-
(ext 532); fax, (949) 362-2049; e-mail, reprints@aacn.org. ment of VAP.

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Within 48 hours of admission to the intensive care medical respiratory ICU at Virginia Commonwealth
unit (ICU), patients have changes in oral flora to pre- University Health Systems in Richmond, Va. This 12-bed
dominantly gram-negative organisms, which include unit has about 1000 admissions each year; approxi-
more virulent organisms.12,13 Dental plaque can pro- mately 50% of the patients admitted require mechani-
vide an environment for microorganisms that cause cal ventilation.
VAP, and dental plaque of patients in the ICU can be All patients admitted to the unit were reviewed for
colonized by potential respiratory pathogens such as potential enrollment in the study. Patients receiving
methicillin-resistant S aureus and Pseudomonas aerugi- mechanical ventilation were enrolled within 24 hours
nosa.14 In addition, abnormalities in salivary flow may of intubation. Because reintubation increases the risk
place patients at risk for overgrowth of organisms in for VAP,19,20 patients who already had had endotracheal
the oropharynx. Circulation of saliva in the mouth intubation during the current hospital admission were
provides mechanical removal of debris and plaque, excluded. Data were obtained during a period of up to
and saliva contains both innate and specific immune 7 days or until extubation. Because clinical evidence
components active in controlling oral microorgan- of VAP occurs after 48 hours of intubation, data on
isms.15-18 Thus, salivary volume and amounts of sali- VAP and oral health were collected on days 1 (base-
vary immune components such as lactoferrin and line), 4, and 7.
immunoglobulin A may influence oropharyngeal colo-
nization and development of VAP. Tubes traversing the Measurement and Quantification of Key Variables
oral cavity that keep the mouth open may contribute to Oral Health Status. Evaluation of oral health sta-
the accumulation of dental plaque by exacerbating tus had 5 components:
xerostomia (dry mouth). Many medications also reduce 1. a baseline count of decayed, missing, and filled
salivary flow. teeth;
2. an assessment of the oral cavity;
3. a culture of an oral specimen;
4. measurement of salivary volume; and
The bacteria found in dental plaque may 5. analysis of 2 salivary immune components:
cause ventilator-associated pneumonia. immunoglobulin A and lactoferrin.
Assessment of the oral cavity consisted of visually
scoring 9 components:
1. dental plaque,
Oral health status in critically ill adults is an impor- 2. inflammation,
tant issue, but it has not been well studied. The specific 3. bleeding,
aim of this study was to describe the relationship 4. purulence,
between oral health status and the development of VAP. 5. candidiasis,
Specifically, we examined the relationship between oral 6. calculus,
health status, as indicated by assessment of the oral 7. stain,
cavity, cultures of oral specimens, salivary volume, and 8. caries, and
salivary immune components, and development of 9. salivary flow (observed salivary volume).
VAP, as indicated by the Clinical Pulmonary Infection The assessments were documented by using a 100-
Score (CPIS). In addition, we determined changes in mm visual analog scale (VAS) for each component.
oral health status during the first 7 days of intubation These components were chosen on the basis of previ-
and mechanical ventilation and the relationships ous work21,22 and were developed in conjunction with a
between microbial colonization of the oropharynx and dental hygiene faculty member and a biostatistician.
colonization of the trachea over time. Salivary flow determined by using the VAS was
significantly correlated with the objective measure-
Methods ment of salivary volume (r = 0.70; P = .006). Number
Design and Sample of teeth decayed was significantly correlated with
A nonexperimental, longitudinal, descriptive design VAS caries (r = 0.83; P < .001). In addition, VAS items
was used. The study was approved by the Virginia not expected to change over time were highly corre-
Commonwealth University Office of Research Sub- lated on different days (caries, r = 0.90, P < .001; stain,
jects Protection and was carried out in accordance r = 0.94, P < .001). This assessment tool provided
with the ethical standards set forth in the Helsinki greater discrimination than categorical scoring sys-
Declaration of 1975. Subjects were recruited from the tems do; data collectors were extensively trained and

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were periodically retested to maintain interrater relia- Several other risk factors may contribute to the
bilities greater than 0.90. development of VAP. Descriptive data related to these
Cultures of oral specimens were evaluated micro- risk factors also were collected, including demograph-
scopically (Gram stain) and semiquantitatively. Each cul- ics and severity of illness as determined by scores on
ture was scored on a 3-point scale identical to the CPIS the Acute Physiology and Chronic Health Evaluation
scale used to describe cultures of tracheal aspirates: (APACHE) II. Demographic data included sex, race,
1 = no growth or few bacteria, age, previous use of antibiotics, reason for intubation,
2 = moderate or large number of bacteria, and type of intubation, intubation process, and reason for
3 = large number of bacteria and same bacteria admission to the ICU.
seen on Gram stain.
Procedure
For each patient, if inclusion criteria were met, the
study was explained to the patient’s legally authorized
Oral comfort care did not affect representative and consent was obtained. Data were
pneumonia risk. collected from time of enrollment in the study through
day 7 of intubation or until extubation. Oral health sta-
tus and CPIS were determined 3 times during the
After the oral assessment, a sample of saliva was study: within 24 hours of intubation (baseline, at time
collected from the sublingual pocket on the dependent of enrollment), at 72 to 96 hours after intubation (dur-
side of the mouth by means of a salivette (Sarstedt ing day 4 of intubation, corresponding to the defini-
Inc, Newton, NC). The salivette was centrifuged to tion of early-onset VAP29), and at 144 to 168 hours
recover the saliva, and the volume of the recovered after intubation (during day 7 of intubation, corre-
saliva was measured. Levels of salivary immunoglob- sponding to late-onset VAP29). Data related to other
ulin A and lactoferrin were determined by using an risk factors for VAP were collected daily and included
enzyme-linked immunosorbent assay (R&D Systems, information on ventilator support, enteral nutrition,
Minneapolis, Minn). Aliquots of saliva samples were and selected medications.
stored at -70ºC until assay. All assays were performed
in triplicate.
Ventilator-Associated Pneumonia. Development
of VAP was determined by using the CPIS.23-25 With As salivary volume decreased, risk of
the CPIS, points are assigned to 6 easily obtained vari- pneumonia increased.
ables:
1. body temperature,
2. white blood cell count,
3. tracheal secretions, Data Analysis
4.oxygenation (ratio of PaO2 to fraction of inspired Descriptive statistics were used to summarize the
oxygen), characteristics of the study population; percentages
5. f indings on chest radiograph (radiologist’s were calculated for discrete variables and means and
report), and SDs for continuous variables. A general forward
6. cultures of tracheal aspirates (microscopic exam- selection multiple regression analysis was used to
ination and semiquantitative culture of tracheal secre- model the relationship between oral health status and
tions, scored by using the same scale as for the oral CPIS at day 4. Day 4 was chosen because the sample
cultures). size at day 7 was small because of loss of patients
Points for each variable of the CPIS are summed, (extubation or death). Variables examined included
yielding a total CPIS (range 0-12), which provides a baseline CPIS, oral assessment scores, salivary vol-
range of scores for data analysis. Although some ume, salivary immunoglobulin A, salivary lactoferrin,
investigators26,27 have used the CPIS as a dichotomous and demographic variables. The final model had the
measure of VAP (CPIS = 6 indicates pneumonia, and highest overall analysis of variance F ratio (F6,21 = 4.86,
CPIS <6 indicates no pneumonia), other investiga- P = .006) and adjusted R2 (R2adj = 0.52). Model param-
tors 12,23,28 have used the entire range of scores to eters are presented in Table 1. Finally, model assump-
describe the clinical development and progression of tions were checked by examining the residual by
pulmonary infection over time. We used the full range predicted plot, the normal quantile plot of the residu-
of scores to describe the risk of VAP. als, and regression diagnostics.

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Table 1 Model parameter estimates Table 2 Characteristics of the sample

Estimate Variable Mean Range


Parameter (SE) t ratio P
Age, y 55 25-93
APACHE 0.172 (0.055) 3.14 .007*
Score on Acute Physiology 20.35 4-41
Salivary volume -0.002 (0.001) -2.61 .02† and Chronic Health
CPIS1 -0.098 (0.202) -0.49 .63 Evaluation II

Plaque 0.005 (0.017) 0.28 .79 No. of decayed teeth 1.08 0-7

CPIS1 × APACHE -0.165 (0.0325) -5.06 <.001* No. of missing teeth 13.85 0-36

CPIS1 × Plaque -0.034 (0.012) -2.76 .01† No. of filled teeth 0.82 0-9
Total No. of decayed, missing, 15.75 0-36
* Significant at P < .01. and filled teeth
† Significant at P < .05.
Abbreviations: APACHE, Acute Physiology and Chronic Health Oral care, No. of times per 2.58 0-7
Evaluation; CPIS, Clinical Pulmonary Infection Score. day

Results given did not affect day 4 CPIS (P = .81) and did not
Characteristics of the Sample differ significantly between patients in whom VAP
The characteristics of the sample are summarized developed and those in whom it did not.
in Table 2. The 66 patients (mean age 55 years, 58% The risk of VAP as evidenced by mean CPIS con-
men) were ethnically diverse: 59% black, 35% white, sistently increased over time (Table 3). Of the 31
3% Asian, and 1.5% Hispanic. Patients remained in patients with complete data through day 4, a total of 8
the study for a mean of 4.2 days. A total of 37 patients (26%) had a score of 6 or higher on the CPIS.
(56%) remained in the study through day 4; 21 (32%),
through day 7. Because patients remained in the study Relationship Between Oral Health Status and VAP
only while intubated and receiving mechanical venti- Factors significantly related to day 4 CPIS were
lation, an important reason for attrition was extubation; APACHE II scores (P = .007), day 4 salivary volume (P
death related to critical illness was another source of = .02), interaction between baseline CPIS and APACHE
attrition. Most of the patients (65%) were intubated II (P < .001), and interaction between baseline CPIS and
because of respiratory failure; the remainder were plaque (P = .01). An inverse relationship was observed
intubated to provide airway control. between salivary volume and day 4 CPIS; as salivary
Baseline counts of decayed, missing, and filled volume decreased, CPIS increased. Because our model
teeth (Table 2) indicated that many patients had oral has 2 interaction terms (baseline CPIS × APACHE II
health problems before admission. Interestingly, the and baseline CPIS × plaque), the effect of plaque on
number of times per day that oral comfort care was day 4 CPIS could not be directly interpreted.

Table 3 Clinical Pulmonary Infection Score (CPIS) and oral health status variables by study day

Baseline Day 4 Day 7


Variable Mean (SD) Mean (SD) Mean (SD)
CPIS 3.66 (1.74) 4.26 (2.02) 4.50 (1.79)
Score on visual analog scale for
oral assessment (millimeters
from zero anchor)
Plaque 21.27 (23.66) 22.72 (20.47) 24.32 (29.01)
Salivary flow 31.86 (28.12) 31.53 (30.95) 26.79 (24.10)
Measured salivary volume, µL 357.2 (483.4) 305.9 (448.4) 133.5 (286.9)*
Immunoglobulin A, g/L 3.5 (4.9) 2.6 (5.8) 3.0 (7.3)
Lactoferrin, µg/mL 398.5 (155.2) 992.5 (181.4) 535.2 (111.0)

* Significant at P < .01.

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28 28 28

26 26 26
APACHE II score

APACHE II score

APACHE II score
24 24 24

22 22 22

20 20 20

18 18 18
1.0 2.0 3.0 4.0 4.5 1.0 2.0 3.0 4.0 4.5 1.0 2.0 3.0 4.0 4.5
CPIS1 CPIS1 CPIS1
Lowest Middle Highest
(cleanest teeth) (most plaque)
Baseline plaque category

Predicted CPIS
0 1 2 3 4 5 6 7 >7

Figure 1 Effect of low (left panel), moderate (middle panel), and high (right panel) amounts of plaque on day 4 Clinical Pul-
monary Infection Score (CPIS) across a range of Acute Physiology and Chronic Health Evaluation (APACHE) II scores for
baseline CPIS <5 (indicating pneumonia was not present at baseline). The contour plots are color keyed such that color wave-
length is associated with day 4 CPIS (larger wavelength indicates higher CPIS); yellow, orange, and red areas correspond to day
CPIS scores ≥ 6 (indicating pneumonia).

The complex relationship between day 4 CPIS and plaque (Figure 1, middle panel) and the most plaque
plaque, APACHE II scores, and baseline CPIS was (Figure 1, right panel), although the breakpoint for
evaluated by using contour plots. In order to generate APACHE II score was 23 in the patients with moderate
the plots, plaque scores were collapsed into 3 cate- plaque and 21 in the patients with the most plaque.
gories: low (cleanest teeth), moderate, and high (most In all categories, when APACHE II and baseline
plaque). Figure 1 shows the relationship of these cate- CPIS were held constant, plaque increases were associ-
gories to day 4 CPIS across a range of APACHE II ated with increased day 4 CPIS. The model indicates
scores for patients who did not have pneumonia at base- that increased plaque was most predictive of pneumo-
line (CPIS <5). The contour plots are keyed so that the nia in patients with high APACHE scores and lower
darkest areas correspond to a day 4 CPIS of 6 or greater baseline CPIS.
(indicating pneumonia). CPIS on day 4 increased as the
APACHE II score increased. Changes in Oral Health Status
During the First 7 Days of Intubation
Data related to oral health status on study days 1
(baseline), 4, and 7 are presented in Tables 3 and 4. Sali-
In the most critically ill, increases in vary volume decreased over time, with significant dif-
dental plaque increased the risk of ferences between day 1 and day 7 (t test, P = .003).
pneumonia. Dental plaque consistently increased over time, although
the differences were not significant. Baseline plaque
score was highly correlated with day 4 plaque score
In patients with the cleanest teeth (Figure 1, left (r = 0.65, P < .001). Baseline salivary lactoferrin was
panel), higher baseline CPIS was predictive of a slight positively correlated with day 4 plaque score (P = .01).
decrease in day 4 CPIS for patients whose APACHE II Other correlations were not significant.
scores were greater than 26. However, for patients
whose APACHE II scores were less than 26, increases Temporal Relationships in Microbial Colonization
in baseline CPIS were predictive of increased day 4 We examined both the concordance between and
CPIS. Similar patterns held for patients with moderate timing of oral and tracheal colonization. The number

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Table 4 Correlations of oral immune variables
Variable By Variable Correlation P
Day 4 plaque Baseline plaque 0.65 <.001*
Day 4 plaque Baseline lactoferrin 0.45 .01†
Baseline immunoglobulin A Baseline lactoferrin -0.13 .36
Day 4 immunoglobulin A Day 4 lactoferrin -0.16 .51
Day 4 plaque Baseline immunoglobulin A 0.26 .18
Day 4 lactoferrin Baseline lactoferrin 0.33 .10
Day 4 Clinical Pulmonary Infection Score Baseline lactoferrin -0.29 .15
Day 4 Clinical Pulmonary Infection Score Baseline immunoglobulin A -0.06 .70

* Significant at P < .01.


† Significant at P < .05.

of organisms present in cultures of oral specimens risk for VAP. Although strong data link certain risk fac-
increased from day 1 to day 4 and remained high on day tors to VAP, the influence of oral health status has not
7 (Figure 2). Potential pathogens were detected in the been examined extensively. We found that the oral health
cultures: S aureus in 4 patients, P aeruginosa in 1 of critically ill patients is often compromised at the time
patient, and Acinetobacter baumanii in 1 patient. Impor- of admission and deteriorates over time, and that a rela-
tantly, in each instance, the organism was present in oral tionship exists between oral health status and VAP.
cultures on the same sampling day or before the appear- The study sample was a diverse group, with African
ance of the organism in cultures of tracheal aspirates. Americans and women well represented. Severity of
We tested the agreement between oral culture illness was appropriate for a large urban medical cen-
scores and tracheal aspirate scores by using a weighted ter, and the VAP rate was similar to the rate reported
κ statistic. The analysis revealed significant agreement in the literature.30 Interestingly, the number of decayed,
on all 3 study days between oral swab score and tra- missing, and filled teeth in our sample is similar to that
cheal aspirate score (day 1, P = .02; day 4, P < .001; reported by Fourrier et al31 (mean 6, SD 8) in a sample
day 7, P = .008). of patients in Europe.
Others have examined dental plaque in ICU patients,
Discussion but we focused exclusively on patients receiving
VAP is associated with increased healthcare costs, mechanical ventilation, restricted the study to the first 7
morbidity, and mortality. Several factors increase the days of intubation, and included oral health status

60
Percentage of cultures

50
scored as 2 or 3

40

30

20

10

0
Oral Tracheal Oral day 4 Tracheal day 4 Oral day 7 Tracheal day 7
Day 1 Day 4 Day 7
Score = 2 Study day
Score = 3

Figure 2 Oral and tracheal specimens for culture were obtained on study days 1, 4, and 7 and were semiquantitatively scored
on a 3-point scale. Columns represent the percentages of oral and tracheal cultures scored 2 and 3.

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parameters other than plaque. In a study by Scannapieco of VAP). Because of the importance of salivary flow
et al,14 a total of 34 patients in a medical respiratory ICU in mechanical removal of oral organisms and in distri-
had mean plaque scores significantly greater than those bution of salivary immune components throughout the
of outpatients in a preventive dentistry clinic. Fourrier oral cavity,15-18 this finding was not surprising. Although
et al31 found an increase over time in dental plaque on our examination was restricted to the first 7 days of
premolar teeth in 15 ICU patients examined on study ventilation, the reduction in salivary volume over time
days 0 and 5. El-Solh et al32 examined dental plaque in might contribute to increases in risk for VAP beyond
49 elderly long-term care residents at the time of the period we studied. Many of the medications given
admission to the ICU and found that dental plaque to critically ill patients (including benzodiazepines,
was worse in those who were subsequently colonized haloperidol, and meperidine) can affect salivary vol-
with respiratory pathogens than in those who were not ume. Methods of increasing oral mucosal hydration
colonized. Scannapieco et al14 did not examine the merit investigation.
relationships between VAP and dental plaque and oral Our data further indicate that levels of innate and
colonization. Fourrier et al31 found that colonization of specific immune components in the mouth, particularly
dental plaque with potential pathogens was signifi- salivary lactoferrin and immunoglobulin A, do change
cantly associated with subsequent nosocomial infec- during critical illness. The role of salivary immune fac-
tions (not limited to VAP). tors has not been thoroughly investigated and might
provide additional insights into risk factors for VAP.
We developed an oral VAS to address difficulties
with previous bedside oral evaluation tools. Our assess-
Good salivary flow enhances the ment tool has tested reliability and validity, includes
removal of oral organisms, reducing multiple parameters of oral health status, and is designed
pneumonia. to evaluate those parameters as continuous measures.
Some of the individual items on the VAS (eg, caries)
are not expected to change during hospitalization; these
items provide a mechanism for ongoing evaluation of
Our data support a link between increases in den- interrater reliability in individual patients or groups of
tal plaque and the development of VAP. The relation- patients. Of note, we were able to maintain a greater
ship was not straightforward but was influenced by than 0.90 interrater reliability throughout the study with
interactions among dental plaque, baseline severity of minimal training.
illness, and baseline pulmonary infection status. The Dental plaque and salivary volume can be deter-
effect of increased plaque was most predictive of pneu- mined by bedside clinicians and are associated with
monia in patients with high APACHE scores and lower risk for VAP. These factors are theoretically amenable
baseline CPIS. The effect of oral care interventions on to alteration by nursing interventions, although oral
VAP has not been shown, but as plaque-reduction care interventions in adults receiving mechanical ven-
interventions are tested, patients who have the highest tilation have not been tested extensively. However, cur-
severity of illness but do not yet have signs of pul- rent oral care is focused on comfort rather on plaque
monary infection might derive the most benefit. The removal or stimulation of salivary flow. We are testing
differential benefits of plaque reduction in particular the effect of specific oral care interventions on removal
subgroups of patients require additional investigation. of plaque and reduction of the incidence of VAP in
Association of plaque scores and risk for VAP may patients in a surgical, medical, and neuroscience ICU.
be due to the potential for dental plaque to harbor
pathogens responsible for VAP in the microbially rich
biofilm. Scannapieco et al,14 Fourrier et al,31 and El-Solh
et al32 all found potential VAP pathogens, including S Optimal oral care should focus on
aureus and P aeruginosa, in the oral cavities of ICU plaque removal and stimulation of
patients. We also cultured these organisms from oral and salivary flow.
tracheal secretions. Potential pathogens were present in
oral specimens at the same time as or before the appear-
ance of the pathogens in tracheal secretions, similar to
the findings in elderly subjects reported by El-Solh et al.32 Oral care interventions that prevent the accumula-
We observed that lower baseline salivary volumes tion of plaque and stimulate local oral immunity dur-
were associated with increased day 4 CPIS (and risk ing the early period of hospitalization might reduce

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development of VAP. These relationships require fur- 15. Kaplan MD, Baum BJ. The functions of saliva. Dysphagia. 1993;8:225-229.
16. Lamkin MS, Oppenheim FG. Structural features of salivary function. Crit
ther examination and might guide the development Rev Oral Biol Med. 1993;4:251-259.
of effective nursing care interventions for prevention 17. Rudney JD, Krig MA, Neuvar EK, Soberay AH, Iverson L. Antimicrobial
proteins in human unstimulated whole saliva in relation to each other, and
of VAP. to measures of health status, dental plaque accumulation and composition.
Arch Oral Biol. 1991;36:497-506.
ACKNOWLEDGMENTS 18. Dawes C. An analysis of factors influencing diffusion from dental plaque into
This research was supported by grants from the National Institute of Nursing a moving film of saliva and the implications for caries. J Dent Res. 1989;
Research (R15 NR07730 to MJG) and the A.D. Williams Foundation, Virginia 68:1483-1488.
Commonwealth University (to CLM). 19. Torres A, Aznar R, Gatell JM, et al. Incidence, risk, and prognosis factors of
nosocomial pneumonia in mechanically ventilated patients. Am Rev Respir
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460 AMERICAN JOURNAL OF CRITICAL CARE, September 2006, Volume 15, No. 5 http://ajcc.aacnjournals.org

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Oral Health Status and Development of Ventilator-Associated Pneumonia: A Descriptive
Study
Cindy L. Munro, Mary Jo Grap, R.K. Elswick, Jr, Jessica McKinney, Curtis N. Sessler and Russell S.
Hummel III
Am J Crit Care 2006;15 453-460
Copyright © 2006 by the American Association of Critical-Care Nurses
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