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DOI 10.1007/s00408-011-9297-0

Association Between Pneumonia and Oral Care in Nursing Home


Residents
Ali A. El-Solh

Received: 9 January 2011 / Accepted: 17 April 2011


Springer Science+Business Media, LLC 2011

Abstract Pneumonia remains the leading cause of death demonstrated in randomized controlled trials. Development
in nursing home residents. The accumulation of dental and maintenance of an oral hygiene program is a critical
plaque and colonization of oral surfaces and dentures with step in the prevention of pneumonia. While resources may
respiratory pathogens serves as a reservoir for recurrent be limited in long-term-care facilities, incorporating oral
lower respiratory tract infections. Control of gingivitis and care in daily routine practice helps to reduce systemic
dental plaques has been effective in reducing the rate of diseases and to promote overall quality of life in nursing
pneumonia but the provision of dental care for institu- home residents.
tionalized elderly is inadequate, with treatment often
sought only when patients experience pain or denture Keywords Oral care  Pneumonia  Nursing home 
problems. Direct mechanical cleaning is thwarted by the Chlorhexidine
lack of adequate training of nursing staff and residents
uncooperativeness. Chlorhexidine-based interventions are
advocated as alternative methods for managing the oral Pneumonia in Long-term-care Facilities
health of frail older people; however, efficacy is yet to be
The aging of the United States (US) population has
occurred steadily over the last century, and this trend is
A. A. El-Solh (&)
expected to continue in the coming decades. In 1995, 33
Medical Research, Bldg. 20 (151) VISN02, VA Western
New York Healthcare System, 3495 Bailey Avenue, million people aged 65 and older comprised 13% of the
Buffalo, NY 14215-1199, USA population. By 2030, the percentage of people aged 65 and
e-mail: solh@buffalo.edu older will rise to 20% of the population [1]. Currently,
4.1% of people in the US older than 65 reside in long-term-
A. A. El-Solh
Division of Pulmonary, Critical Care, and Sleep Medicine, care facilities (LTCFs), and 15% of people older than 85
Department of Medicine, State University of New York are nursing home residents [2]. Twelve studies conducted
at Buffalo School of Medicine and Biomedical Sciences in a variety of North American LTCFs since 1978 indicate
and School of Public Health and Health Professions, Buffalo,
that the overall incidence of infections in these facilities
NY, USA
ranges between 1.8 and 13.5 infections per 1,000 resident-
A. A. El-Solh care days [3]. Pneumonia remains the leading cause of
Department of Anesthesiology, State University of New York death attributable to infection in patients aged 65 and older
at Buffalo School of Medicine and Biomedical Sciences and
and accounts for 13-48% of infections in the nursing home
School of Public Health and Health Professions, Buffalo,
NY, USA setting, with mortality rates as high as 55% [4, 5]. The
incidence of pneumonia among residents of LTCFs ranges
A. A. El-Solh from 0.27 to 2.5 per 1,000 patient-days, with a median
Department of Social and Preventive Medicine, State University
reported incidence of 1 per 1,000 patient-days. Expressed
of New York at Buffalo School of Medicine and Biomedical
Sciences and School of Public Health and Health Professions, as annual rates of infection, the reported annual incidence
Buffalo, NY, USA of pneumonia in long-term-care residents ranges from 99 to

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912 per 1,000 persons (median = 365 per 1,000) [6]. In distinction between these two entities and does not impose
comparison, the annual incidence of pneumonia in the a restriction on antimicrobial therapy for those with aspi-
community is approximately 12 per 1,000 persons per year, ration pneumonitis. For all practical purposes, the differ-
rising to 34 per 1,000 in those 75 years of age and older ence between aspiration pneumonia and aspiration
[7]. Two other prospective studies carried out more than pneumonitis remains theoretical in the eyes of practitioners
10 years apart found rates of nursing home acquired and antimicrobial treatment is invariably prescribed for
pneumonia (NHAP) of 1 episode per 1,000 resident care pneumonia irrespective of the underlying pathophysiology.
days and 0.7 episode per 1,000 resident care days [8, 9].
There are several factors that predispose nursing home
residents to respiratory infections. Ineffective clearing of Association Between Oral Health and Respiratory
mucus from the respiratory tract makes older people, Pathogens in Nursing Home Residents
especially those with additional disease burden such as
cerebrovascular accident, dysphagia, gastroesophageal There are several avenues by which potential pathogens
reflux disease, presbyesophagus, or sedative-hypnotic may gain access to the lower respiratory tract: (1) aspira-
medication use, more vulnerable to pneumonia [10, 11]. tion of the oropharyngeal contents, (2) inhalation of
Institutionalized individuals are at particularly high risk for infectious aerosols, (3) spread of infection from contiguous
severe consequences of pneumonia due to decreased sites, and (4) hematogenous spread from extrapulmonary
respiratory reserve, presence of comorbid diseases such as sites of infection. Colonization of the oral cavity followed
chronic obstructive pulmonary disease, diabetes mellitus, by aspiration of bacteria-laden oropharyngeal secretions
and coronary artery disease, and the waning of innate and into the lower respiratory tract remains the most common
specific immunity that occurs with aging. In addition, the path of infection for typical bacterial pneumonia [15].
more widespread use of an array of immunosuppressive Indeed, it has long been recognized that anaerobic lung
drugs, such as corticosteroids, and cytotoxic agents to treat infections can occur following aspiration of salivary
autoimmune, inflammatory, or malignant disorders has secretions, especially in patients with periodontal disease
likely increased the frequency and severity of pneumonia. [16, 17]. Quagliarello et al. [18] found poor oral hygiene to
Several preventive measures, including influenza and be among the most common risk factors of pneumonia in
pneumococcal vaccinations, have been linked to substantial nursing homes. Nine modifiable risk factors for NHAP
reduction in illnesses in recent years, yet the incidence of were examined in 613 elderly patients at a nursing home,
pneumonia remains unchanged or even continues to rise in including inadequate oral care, difficulty in swallowing,
some age groups [12]. lack of influenza vaccination, depression, feeding position
There are two pneumonic aspiration syndromes that are of less than 90 from horizontal, active smoking, receipt of
described in the literature that are most applicable to sedative medication, receipt of gastric acid-reducing med-
nursing home residents [13]. Aspiration pneumonitis is a ication, and use of angiotensin-converting enzyme inhibi-
noninfectious process secondary to macroaspiration of tors. The only two risk factors that were shown to have
food, regurgitated acid, or particulate matter. These cases significant association with risk of developing pneumonia
vary in severity. Some episodes may exhibit a protracted were inadequate oral care and difficulty swallowing [18].
course and end up in death, while others may resolve Patients with periodontal disease harbor a large number
rapidly. Aspiration pneumonia is an infectious process of subgingival bacteria, including anaerobic and fastidious
secondary to oropharyngeal dysphagia with inhalation of species. Langmore et al. [19] identified high levels of the
periodontal bacteria or pharyngeal colonizers or due to periodontal pathogen Porphyromonas gingivalis and
regurgitation of colonized gastric material. It has been Streptococcus sobrinus in the oral cavity of elderly. These
argued that while aspiration pneumonia requires antimi- are the same organisms implicated in the etiology of
crobial therapy, aspiration pneumonitis does not. Yet, pneumonia from patients associated with poor oral
practicing providers do not make this distinction for the hygiene. In another study of 500 adults with refractory
following reasons: First, there is no clinical or biological periodontitis, enteric rods and pseudomonads were cultured
marker that would differentiate these two entities; second, from subgingival sites in over 10% of the subjects [20]. A
there is always the plausibility that these two entities may follow-up clinical investigation found 14% of patients with
overlap. In this case, the risk of withholding antimicrobial periodontitis to harbor enteric rods and/or Pseudomonas
therapy in a frail population outweighs the risk of over- species in subgingival dental plaque [21]. Cantrell [22]
treatment with antibiotics. Mylotte et al. [14] have devel- asserted a well-documented role between severe gingi-
oped an algorithm to distinguish between aspiration val disease, heavy calculus deposition, and anaerobic
pneumonitis and aspiration pneumonia but the model had pleuropulmonary disease, specifically pneumonia. In a
no microbiological documentation to substantiate a series of cases of anaerobic pleuropulmonary disease, there

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was a significantly greater prevalence of periodontal hygiene at nursing home facilities. Patients with severe
infection than among age-matched controls [23]. In par- dementia have the worst oral hygiene and the largest
ticular, an increased prevalence of P. gingivalis and Bac- number of nonrestorable carious teeth. Members of this
teroides forsythus, two known periodontal pathogens, were group are also less capable of describing oral symptoms, so
isolated from patients with anaerobic pleuropulmonary conditions can easily deteriorate without clinical inter-
disease. vention. Analysis of the degree of functional dependency
Institutionalized subjects appear to be more prone to revealed that there was no significant difference between
substantial oral colonization by respiratory pathogens than the ages of those accepting or refusing dental care [32]. In
are ambulatory, noninstitutionalized subjects when mat- fact, nursing home residents who are more dependent are
ched for age, gender, race, and comorbid conditions. The no less receptive to dental treatment than residents who are
mean percentage of aerobic flora composed of respiratory more independent. Of the residents assessed, more than
pathogens in chronic care facility subjects was 71% expressed willingness to receive dental care [32]. This
37.5 44.9%, while in dental outpatient subjects the mean finding suggests a higher than expected level of demand for
level was only 0.02 0.04% (p = 0.04) [24]. Among the dental care among institutionalized elders. It also indicates
respiratory pathogens isolated, Staphylococcus aureus, that functionally dependent elderly are retaining their teeth
Pseudomonas aeruginosa, Klebsiella pneumoniae, Enter- longer.
obacter cloacae, and Escherichia coli were the prevalent The first conclusive evidence linking oral microbes to
microorganisms. A similar study examined dental plaque pneumonia was derived from a prospective study con-
as the source for potential pathogenic organisms that may ducted in 2004 [33]. Forty-nine institutionalized elderly
cause respiratory disease in nursing home residents [25]. requiring mechanical ventilation underwent oral examina-
Of the 138 residents examined, 89 subjects presented with tion and dental sampling on admission to the intensive care
potential respiratory pathogens colonized from their dental unit. Thirty-three respiratory pathogens were identified
plaque. Twenty-one species of microorganisms were from the dental plaques. Fourteen patients (29%) subse-
detected in the dental plaque, and the predominant poten- quently developed clinical evidence of pneumonia during
tial respiratory pathogens detected in these plaques were hospitalization. Nine respiratory pathogens isolated from
Staphylococcus aureus, Klebsiella pneumoniae, Pseudo- the lower respiratory tract matched genetically those
monas aeruginosa, and Enterobacter cloacae. The release recovered from dental plaques. The results of the study
of trypsin-like proteases (TLPs) and neuraminidase (NA) convincingly demonstrated that respiratory pathogens from
by these respiratory pathogens plays also a major role in the lung are often genetically indistinguishable from strains
facilitating influenza infection [26, 27], the leading cause isolated from the oral cavity and that dental plaques serve
of death in older adults. as an important reservoir for respiratory pathogens in these
More than two decades after the publication of the oral patients. These findings confirmed the conclusions of
health survey of long-term patients in the VA health-care Scannapieco et al. [34] who reported an overall relative
system [28], a recent analysis of 143 residents of a Vet- risk of pneumonia of 9.6 when dental plaque was colonized
erans Affairs Medical Center nursing home again noted and a significant association between decayed teeth
poor oral care overall as reflected by a higher degree of (OR = 1.2), dental plaque (OR = 4.2), and dependency
plaque and debris scores [29]. These results suggest that for oral care (OR = 2.8).
institutionalized subjects have a greater tendency for dental A recent study from Japan summarized these observa-
plaque colonization by respiratory pathogens [18, 30, 31]. tions by showing a significant association between dental
Table 1 lists potential risk factors implicated in poor oral disease and mortality-related aspiration pneumonia. Awano
and coworkers [35] showed that the adjusted mortality due
Table 1 Risk factors associated
to pneumonia was 3.9 times higher in persons with ten or
Poor diabetic control more teeth with a probing depth exceeding 4 mm (peri-
with poor oral care in nursing
homes Advanced malignancy odontal pocket) than in those without periodontal pockets.
Impaired swallowing reflex In a recent systematic review, it was estimated that
Dementia approximately one in ten cases of death from pneumonia in
Cerebrovascular accident elderly nursing home residents may be prevented by
Parkinsons disease
improving oral hygiene [36].
Radiation therapy
Unfortunately, regimens for enhancing oral hygiene at
Human immunodeficiency virus
LTCFs, where physical dependency often requires assis-
tance in activities of daily living be provided by a care-
Poor functional status
giver, have largely been ignored. While limited controlled
Drug-induced xerostomia
studies, in both scope and sample size, have identified this

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problem, the effectiveness of programs for improving the coverage is curtailed under the Medicare and Medicaid
oral health in nursing homes have not been thoroughly programs because the majority of dental services are
investigated. viewed as not medically necessary. Traditionally, Medicare
provides coverage for acute care only, which generally
Effects of Edentulism does not include dental coverage. In the rare instances
where Medicare will provide dental coverage, the dental
The microbial flora of edentulous elderly subjects is sub- procedure must be linked to an underlying health condition.
stantially different from dentate subjects [37]. Obviously, As a result, reimbursement for oral care under the Medi-
people without teeth would not be affected by periodontal care and the Medicaid program is severely limited and
inflammation. A recent study showed that dentate elderly poorly funded.
individuals have a higher risk of harboring periodonto-
pathic pathogens than those who are edentulous (91.4% vs.
40.3%, p \ 0.001) [38]. However, periodontal pathogens Effectiveness of Oral Care Intervention Programs
may persist in the oral cavity of edentulous subjects who
have had periodontal disease for an extended period of time The most compelling evidence obtained to date supporting
after the extraction of all teeth and in the absence of other the effectiveness of oral care comes from several inter-
hard surfaces in the mouth [39]. The current evidence ventional studies that have demonstrated a reduction in
suggests that the prevalence of respiratory tract infection is lower respiratory tract infections following improvement in
significantly greater among dentate than edentulous sub- oral hygiene (Table 2).
jects (40% vs. 27%) and is also greater among subjects
with selected oral disorders than those without such con- Mechanical Intervention
ditions [31, 40]. Similarly, Terpenning et al. [41] found a
trend toward lower prevalence of pneumonia among In a randomized study of elderly nursing home patients,
edentulous elderly patients. However, Yoneyama and Yoneyama et al. [42] randomized 417 patients to an oral
coworkers [42] showed that even in edentate patients, care group or no oral care group. In the oral care group,
fever, nonfatal pneumonia, and fatal pneumonia occurred nurses or caregivers cleaned the patients teeth with a
less frequently in the group assigned to enhanced oral care toothbrush for approximately 5 min after each meal. The
compared to the group assigned to routine oral care (18, 9, brushing was performed as usual daily tooth brushing,
and 7% vs. 34, 20, and 13%, respectively). Abe et al. [43] including brushing palatal and mandibular mucosa and
raised the possibility that bacterial tongue-coating might tongue dorsum. If the toothbrush was not efficient, the
represent another source of aspiration pneumonia in oropharynx was scrubbed with an applicator with povidone
edentate subjects, making the argument that not only the iodine (1%). In the no oral care group, patients performed
dentate elderly should be targeted for oral cleaning. tooth brushing by themselves irregularly. During a 2-year
follow-up, the incidence of pneumonia in the oral group
Barriers to Oral Care decreased from 19 to 11%. Mortality from pneumonia was
also about half that in patients not receiving oral care. The
There are major barriers to oral care for patients in nursing study was criticized for lack of blinding, failure to adjust
homes. These include the lack of specific designated per- for comorbidities, and the absence of a standard practice of
sonnel to perform oral care, lack of adequate training of oral care in the control group. More significantly, the oral
nursing staff, resident noncompliance with care, and choice care regimen implemented on those randomized to the
of oral care itself [44, 45]. In a survey of 14 nursing homes treatment arm was both too stringent and labor-intensive,
in Virginia, patient uncooperativeness was listed as the which made it impractical to be recommended as a stan-
major factor in whether oral services were provided [46]. dard of care for institutionalized subjects. In a similar
Coleman [45] reiterated these findings in an observational study, Adachi and coworkers [48] compared the effec-
study of a group of nursing home patients with dementia. tiveness of weekly professional oral health care given by
However, in a separate investigation, over 70% of nursing dental hygienists to 77 residents of a long-term-care facility
home residents indicated that they had not seen a dentist for compared to 64 residents who did not receive professional
over 5 years and 82% of denture wearers were unable to oral health care. The prevalence of fevers of 37.8C or
clean their denture [47]. Yet none received regular assis- more and the rate of fatal aspiration pneumonia in the
tance. While the staff had a good understanding of the role subjects receiving professional oral health care were sig-
of oral care in preventing dental disease, only one third had nificantly lower (4% and 5% vs. 7% and 16.7%, respec-
received training in oral health or instructions on how to tively; p \ 0.05). Of interest, 49 patients were not included
provide oral care. To complicate the matter more, dental in the final analysis because of dementia and another 14

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Table 2 Effectiveness of oral care in reducing risk of pneumonia in nursing home residents
Ref. Population Design Intervention Outcomes

Yoneyama et al. 417 NH residents Randomized controlled trial Daily tooth brushing plus RR of developing pneumonia 1.67
[42] over 2-year period scrubbing of pharynx with in the group on no oral care
povidone iodine 1% (including compared with oral care
professional care once a week) (p = 0.04)
vs. routine oral care
Simons et al. [59] 111 dentate elderly Double-blind, randomized CHX/xylitol gum vs. xylitol Significant reduction in denture
controlled trial over (X) gum vs. no gum debris, stomatitis, and cheilitis in
12-month period CHX/X and X groups compared
to no gum
Ueda et al. [49] 105 long-term-care Prospective interventional Oral care intervention at intervals Oral hygienic condition could be
residents study of 1, 2, 3, 4, and 6 weeks improved by performing oral
care at intervals of 1 week for 12
consecutive weeks, and
maintained at intervals of 1 week
thereafter
Abe et al. [50] 190 elderly patients Prospective, randomized Weekly professional oral care RR of developing influenza while
for 6 months versus self oral care under professional oral care
compared to that in the control
group was 0.1 (95% CI 0.01-
0.81, p = 0.008)
Adachi et al. [62] 216 NH residents Prospective interventional Daily routine oral care plus either Fatal aspiration pneumonia
study over 24 months mechanical cleaning weekly vs. (RR = 2.67; p \ 0.5) higher in
basic oral hygiene (swabbing and those who did not receive
denture cleaning) professional oral care compared
to interventional group
Ishikawa et al. 202 NH residents Prospective interventional Professional oral care weekly vs. Professional oral care decreased
[63] study over 5-month gargling with 0.35% povidone burden of oropharyngeal bacteria
period iodine daily vs. no professional and was more effective than
care gargling with povidone iodine
Bassim et al. [29] 143 NH residents Retrospective review up to Assisted oral hygiene Odds ratio for dying from
79 weeks (toothbrushing, antiseptic mouth pneumonia 3.57 higher in the
wash) vs. no assisted oral care control group than the oral
hygiene group
NH nursing home, CHX chlorhexidine, RR relative risk

dropped out of the study during the study period. In order tenfold in those assigned to professional oral cleaning
to determine the optimal frequency of professional inter- (p = 0.008).
vention by dental health-care workers, Ueda et al. [49] A recent study involving 143 residents of a nursing
showed that oral hygienic condition could be improved by home investigated the association between the assignment
performing professional oral care in which an interdental of an oral hygiene aide staff member and mortality from
toothbrush, an engine brush, and a scaler were used for pneumonia [29]. The oral care provided by the nursing
tooth cleaning at an interval of 1 week for 12 consecutive home oral hygiene aides included setting up for, encour-
weeks. The improved condition could be maintained when aging, and monitoring self oral hygiene care for all resi-
professional oral care was continued at a 1-week interval dents who were aware and able to participate in their own
thereafter. care. This included tooth brushing, antiseptic mouthwash
The benefit of oral care has also been shown to translate use, and oral and denture cleaning for edentulous or par-
into a reduction in influenza infection. Abe et al. [50] tially edentulous residents. For patients who were unable to
assigned randomly 190 elderly patients to either profes- perform oral care, the aides would provide this care
sional oral care once a week or to self-care. The intervention directly. Looking at the records up to 79 weeks retro-
group had a significant drop in bacteria colony-forming spectively, patients in the oral care group had significantly
units (CFUs), NA, and TLPs compared to the control group, lower plaque and debris scores (using the Simplified Oral
and the rate of developing influenza was reduced by Hygiene Index) than did patients in the no oral care group.

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When the data were adjusted for risk factors found to be showed that cough reflex sensitivity at 30 days in those with
significant for mortality from pneumonia, the odds of dying intensive oral hygiene measures (intervention) was signifi-
from pneumonia in the group that did not receive oral care cantly higher than in the control (no intervention) group.
was more than three times that of the group that did receive The odds ratio for improvement of cough reflex was 5.3 in
oral care (OR = 3.57, p = 0.03). However, the non-ran- the intervention group compared with the control group;
domized controlled trial studies contributed to inconclusive however, no significant effect was seen with respect to
evidence on the association and correlation between oral serum substance P, cognitive function, and activities of
hygiene and pneumonia or respiratory tract infection in daily living. The authors concluded that intensive oral
elderly people. hygiene measures might reduce the incidence of pneumonia
by improving cough reflex sensitivity in the elderly. How-
Chemical Intervention ever, pneumonia was not included among the end points.
Nonetheless, the result of this study supports the need for
It is not always possible for disabled nursing home resi- oral health-care interventions and indicates that improved
dents to brush their teeth or their dentures effectively, oral care may reduce the incidence of pneumonia.
hence chemical solutions for removing plaques and disin-
fecting acrylic resin became an alternative for mechanical
oral care in this population. Among these agents, chlorh- Conclusion
exidine appeared on the market in mid-1970 s for use by
individuals undergoing periodontal treatment and dental The current review finds strong support for the need to
implant surgery. Chlorhexidine has bactericidal, fungicidal, implement a program that uses oral hygiene in the long-
and some virus-killing properties. When used topically, the term-care setting as part of daily routine. With skyrocketing
N-chlorinated derivative of chlorhexidine binds covalently health-care costs and the increasing incidence of aspiration
to proteins in the skin and mucosa and results in a persis- pneumonia in the aging population, dental hygiene repre-
tent antimicrobial effect with limited systemic absorption, sents an effective cost-saving intervention. Programs to
even after an oral ingestion. Compared to other antiseptics, improve oral health-care knowledge and skills, delivered by
chlorhexidine is superior to Listerine and Meridol in its dental professionals, must be included in the curricula of all
ability to maintain low plaque scores and gingival health nurse-training establishments. In addition, programs for
during a 3-week period of no mechanical oral hygiene [51, practical training of care assistants in basic oral health care
52]. Although decreased susceptibility to chlorhexidine has need to be actively promoted in nursing homes. There is
been reported, it has not been convincingly shown to be also an urgent need for randomized controlled studies to
associated with repeated exposure to chlorhexidine [53]. determine the optimal regimen(s) of an oral hygiene pro-
Oral ingestion of chlorhexidine is usually well tolerated gram in the prevention of NHAP [61].
because negligible systemic absorption occurs.
The effectiveness of oral chlorhexidine in reducing
respiratory tract infections has been examined in a number
of critical care studies with conflicting results [5458]. The References
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