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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


in nursing home residents. The accumulation of dental
plaque and colonization of oral surfaces and dentures with
respiratory pathogens serves as a reservoir for recurrent
lower respiratory tract infections. Control of gingivitis and
dental plaques has been effective in reducing the rate of
pneumonia but the provision of dental care for institutionalized elderly is inadequate, with treatment often
sought only when patients experience pain or denture
problems. Direct mechanical cleaning is thwarted by the
lack of adequate training of nursing staff and residents
uncooperativeness. Chlorhexidine-based interventions are
advocated as alternative methods for managing the oral
health of frail older people; however, efficacy is yet to be
A. A. El-Solh (&)
Medical Research, Bldg. 20 (151) VISN02, VA Western
New York Healthcare System, 3495 Bailey Avenue,
Buffalo, NY 14215-1199, USA
e-mail: solh@buffalo.edu
A. A. El-Solh
Division of Pulmonary, Critical Care, and Sleep Medicine,
Department of Medicine, State University of New York
at Buffalo School of Medicine and Biomedical Sciences
and School of Public Health and Health Professions, Buffalo,
NY, USA
A. A. El-Solh
Department of Anesthesiology, State University of New York
at Buffalo School of Medicine and Biomedical Sciences and
School of Public Health and Health Professions, Buffalo,
NY, USA
A. A. El-Solh
Department of Social and Preventive Medicine, State University
of New York at Buffalo School of Medicine and Biomedical
Sciences and School of Public Health and Health Professions,
Buffalo, NY, USA

demonstrated in randomized controlled trials. Development


and maintenance of an oral hygiene program is a critical
step in the prevention of pneumonia. While resources may
be limited in long-term-care facilities, incorporating oral
care in daily routine practice helps to reduce systemic
diseases and to promote overall quality of life in nursing
home residents.
Keywords Oral care  Pneumonia  Nursing home 
Chlorhexidine

Pneumonia in Long-term-care Facilities


The aging of the United States (US) population has
occurred steadily over the last century, and this trend is
expected to continue in the coming decades. In 1995, 33
million people aged 65 and older comprised 13% of the
population. By 2030, the percentage of people aged 65 and
older will rise to 20% of the population [1]. Currently,
4.1% of people in the US older than 65 reside in long-termcare facilities (LTCFs), and 15% of people older than 85
are nursing home residents [2]. Twelve studies conducted
in a variety of North American LTCFs since 1978 indicate
that the overall incidence of infections in these facilities
ranges between 1.8 and 13.5 infections per 1,000 residentcare days [3]. Pneumonia remains the leading cause of
death attributable to infection in patients aged 65 and older
and accounts for 13-48% of infections in the nursing home
setting, with mortality rates as high as 55% [4, 5]. The
incidence of pneumonia among residents of LTCFs ranges
from 0.27 to 2.5 per 1,000 patient-days, with a median
reported incidence of 1 per 1,000 patient-days. Expressed
as annual rates of infection, the reported annual incidence
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


comparison, the annual incidence of pneumonia in the
community is approximately 12 per 1,000 persons per year,
rising to 34 per 1,000 in those 75 years of age and older
[7]. Two other prospective studies carried out more than
10 years apart found rates of nursing home acquired
pneumonia (NHAP) of 1 episode per 1,000 resident care
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
mucus from the respiratory tract makes older people,
especially those with additional disease burden such as
cerebrovascular accident, dysphagia, gastroesophageal
reflux disease, presbyesophagus, or sedative-hypnotic
medication use, more vulnerable to pneumonia [10, 11].
Institutionalized individuals are at particularly high risk for
severe consequences of pneumonia due to decreased
respiratory reserve, presence of comorbid diseases such as
chronic obstructive pulmonary disease, diabetes mellitus,
and coronary artery disease, and the waning of innate and
specific immunity that occurs with aging. In addition, the
more widespread use of an array of immunosuppressive
drugs, such as corticosteroids, and cytotoxic agents to treat
autoimmune, inflammatory, or malignant disorders has
likely increased the frequency and severity of pneumonia.
Several preventive measures, including influenza and
pneumococcal vaccinations, have been linked to substantial
reduction in illnesses in recent years, yet the incidence of
pneumonia remains unchanged or even continues to rise in
some age groups [12].
There are two pneumonic aspiration syndromes that are
described in the literature that are most applicable to
nursing home residents [13]. Aspiration pneumonitis is a
noninfectious process secondary to macroaspiration of
food, regurgitated acid, or particulate matter. These cases
vary in severity. Some episodes may exhibit a protracted
course and end up in death, while others may resolve
rapidly. Aspiration pneumonia is an infectious process
secondary to oropharyngeal dysphagia with inhalation of
periodontal bacteria or pharyngeal colonizers or due to
regurgitation of colonized gastric material. It has been
argued that while aspiration pneumonia requires antimicrobial therapy, aspiration pneumonitis does not. Yet,
practicing providers do not make this distinction for the
following reasons: First, there is no clinical or biological
marker that would differentiate these two entities; second,
there is always the plausibility that these two entities may
overlap. In this case, the risk of withholding antimicrobial
therapy in a frail population outweighs the risk of overtreatment with antibiotics. Mylotte et al. [14] have developed an algorithm to distinguish between aspiration
pneumonitis and aspiration pneumonia but the model had
no microbiological documentation to substantiate a

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distinction between these two entities and does not impose


a restriction on antimicrobial therapy for those with aspiration pneumonitis. For all practical purposes, the difference between aspiration pneumonia and aspiration
pneumonitis remains theoretical in the eyes of practitioners
and antimicrobial treatment is invariably prescribed for
pneumonia irrespective of the underlying pathophysiology.

Association Between Oral Health and Respiratory


Pathogens in Nursing Home Residents
There are several avenues by which potential pathogens
may gain access to the lower respiratory tract: (1) aspiration of the oropharyngeal contents, (2) inhalation of
infectious aerosols, (3) spread of infection from contiguous
sites, and (4) hematogenous spread from extrapulmonary
sites of infection. Colonization of the oral cavity followed
by aspiration of bacteria-laden oropharyngeal secretions
into the lower respiratory tract remains the most common
path of infection for typical bacterial pneumonia [15].
Indeed, it has long been recognized that anaerobic lung
infections can occur following aspiration of salivary
secretions, especially in patients with periodontal disease
[16, 17]. Quagliarello et al. [18] found poor oral hygiene to
be among the most common risk factors of pneumonia in
nursing homes. Nine modifiable risk factors for NHAP
were examined in 613 elderly patients at a nursing home,
including inadequate oral care, difficulty in swallowing,
lack of influenza vaccination, depression, feeding position
of less than 90 from horizontal, active smoking, receipt of
sedative medication, receipt of gastric acid-reducing medication, and use of angiotensin-converting enzyme inhibitors. The only two risk factors that were shown to have
significant association with risk of developing pneumonia
were inadequate oral care and difficulty swallowing [18].
Patients with periodontal disease harbor a large number
of subgingival bacteria, including anaerobic and fastidious
species. Langmore et al. [19] identified high levels of the
periodontal pathogen Porphyromonas gingivalis and
Streptococcus sobrinus in the oral cavity of elderly. These
are the same organisms implicated in the etiology of
pneumonia from patients associated with poor oral
hygiene. In another study of 500 adults with refractory
periodontitis, enteric rods and pseudomonads were cultured
from subgingival sites in over 10% of the subjects [20]. A
follow-up clinical investigation found 14% of patients with
periodontitis to harbor enteric rods and/or Pseudomonas
species in subgingival dental plaque [21]. Cantrell [22]
asserted a well-documented role between severe gingival disease, heavy calculus deposition, and anaerobic
pleuropulmonary disease, specifically pneumonia. In a
series of cases of anaerobic pleuropulmonary disease, there

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was a significantly greater prevalence of periodontal


infection than among age-matched controls [23]. In particular, an increased prevalence of P. gingivalis and Bacteroides forsythus, two known periodontal pathogens, were
isolated from patients with anaerobic pleuropulmonary
disease.
Institutionalized subjects appear to be more prone to
substantial oral colonization by respiratory pathogens than
are ambulatory, noninstitutionalized subjects when matched for age, gender, race, and comorbid conditions. The
mean percentage of aerobic flora composed of respiratory
pathogens in chronic care facility subjects was
37.5 44.9%, while in dental outpatient subjects the mean
level was only 0.02 0.04% (p = 0.04) [24]. Among the
respiratory pathogens isolated, Staphylococcus aureus,
Pseudomonas aeruginosa, Klebsiella pneumoniae, Enterobacter cloacae, and Escherichia coli were the prevalent
microorganisms. A similar study examined dental plaque
as the source for potential pathogenic organisms that may
cause respiratory disease in nursing home residents [25].
Of the 138 residents examined, 89 subjects presented with
potential respiratory pathogens colonized from their dental
plaque. Twenty-one species of microorganisms were
detected in the dental plaque, and the predominant potential respiratory pathogens detected in these plaques were
Staphylococcus aureus, Klebsiella pneumoniae, Pseudomonas aeruginosa, and Enterobacter cloacae. The release
of trypsin-like proteases (TLPs) and neuraminidase (NA)
by these respiratory pathogens plays also a major role in
facilitating influenza infection [26, 27], the leading cause
of death in older adults.
More than two decades after the publication of the oral
health survey of long-term patients in the VA health-care
system [28], a recent analysis of 143 residents of a Veterans Affairs Medical Center nursing home again noted
poor oral care overall as reflected by a higher degree of
plaque and debris scores [29]. These results suggest that
institutionalized subjects have a greater tendency for dental
plaque colonization by respiratory pathogens [18, 30, 31].
Table 1 lists potential risk factors implicated in poor oral
Table 1 Risk factors associated
with poor oral care in nursing
homes

Poor diabetic control


Advanced malignancy
Impaired swallowing reflex
Dementia
Cerebrovascular accident
Parkinsons disease
Radiation therapy
Human immunodeficiency virus
Poor functional status
Drug-induced xerostomia

hygiene at nursing home facilities. Patients with severe


dementia have the worst oral hygiene and the largest
number of nonrestorable carious teeth. Members of this
group are also less capable of describing oral symptoms, so
conditions can easily deteriorate without clinical intervention. Analysis of the degree of functional dependency
revealed that there was no significant difference between
the ages of those accepting or refusing dental care [32]. In
fact, nursing home residents who are more dependent are
no less receptive to dental treatment than residents who are
more independent. Of the residents assessed, more than
71% expressed willingness to receive dental care [32]. This
finding suggests a higher than expected level of demand for
dental care among institutionalized elders. It also indicates
that functionally dependent elderly are retaining their teeth
longer.
The first conclusive evidence linking oral microbes to
pneumonia was derived from a prospective study conducted in 2004 [33]. Forty-nine institutionalized elderly
requiring mechanical ventilation underwent oral examination and dental sampling on admission to the intensive care
unit. Thirty-three respiratory pathogens were identified
from the dental plaques. Fourteen patients (29%) subsequently developed clinical evidence of pneumonia during
hospitalization. Nine respiratory pathogens isolated from
the lower respiratory tract matched genetically those
recovered from dental plaques. The results of the study
convincingly demonstrated that respiratory pathogens from
the lung are often genetically indistinguishable from strains
isolated from the oral cavity and that dental plaques serve
as an important reservoir for respiratory pathogens in these
patients. These findings confirmed the conclusions of
Scannapieco et al. [34] who reported an overall relative
risk of pneumonia of 9.6 when dental plaque was colonized
and a significant association between decayed teeth
(OR = 1.2), dental plaque (OR = 4.2), and dependency
for oral care (OR = 2.8).
A recent study from Japan summarized these observations by showing a significant association between dental
disease and mortality-related aspiration pneumonia. Awano
and coworkers [35] showed that the adjusted mortality due
to pneumonia was 3.9 times higher in persons with ten or
more teeth with a probing depth exceeding 4 mm (periodontal pocket) than in those without periodontal pockets.
In a recent systematic review, it was estimated that
approximately one in ten cases of death from pneumonia in
elderly nursing home residents may be prevented by
improving oral hygiene [36].
Unfortunately, regimens for enhancing oral hygiene at
LTCFs, where physical dependency often requires assistance in activities of daily living be provided by a caregiver, have largely been ignored. While limited controlled
studies, in both scope and sample size, have identified this

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problem, the effectiveness of programs for improving the


oral health in nursing homes have not been thoroughly
investigated.
Effects of Edentulism
The microbial flora of edentulous elderly subjects is substantially different from dentate subjects [37]. Obviously,
people without teeth would not be affected by periodontal
inflammation. A recent study showed that dentate elderly
individuals have a higher risk of harboring periodontopathic pathogens than those who are edentulous (91.4% vs.
40.3%, p \ 0.001) [38]. However, periodontal pathogens
may persist in the oral cavity of edentulous subjects who
have had periodontal disease for an extended period of time
after the extraction of all teeth and in the absence of other
hard surfaces in the mouth [39]. The current evidence
suggests that the prevalence of respiratory tract infection is
significantly greater among dentate than edentulous subjects (40% vs. 27%) and is also greater among subjects
with selected oral disorders than those without such conditions [31, 40]. Similarly, Terpenning et al. [41] found a
trend toward lower prevalence of pneumonia among
edentulous elderly patients. However, Yoneyama and
coworkers [42] showed that even in edentate patients,
fever, nonfatal pneumonia, and fatal pneumonia occurred
less frequently in the group assigned to enhanced oral care
compared to the group assigned to routine oral care (18, 9,
and 7% vs. 34, 20, and 13%, respectively). Abe et al. [43]
raised the possibility that bacterial tongue-coating might
represent another source of aspiration pneumonia in
edentate subjects, making the argument that not only the
dentate elderly should be targeted for oral cleaning.
Barriers to Oral Care
There are major barriers to oral care for patients in nursing
homes. These include the lack of specific designated personnel to perform oral care, lack of adequate training of
nursing staff, resident noncompliance with care, and choice
of oral care itself [44, 45]. In a survey of 14 nursing homes
in Virginia, patient uncooperativeness was listed as the
major factor in whether oral services were provided [46].
Coleman [45] reiterated these findings in an observational
study of a group of nursing home patients with dementia.
However, in a separate investigation, over 70% of nursing
home residents indicated that they had not seen a dentist for
over 5 years and 82% of denture wearers were unable to
clean their denture [47]. Yet none received regular assistance. While the staff had a good understanding of the role
of oral care in preventing dental disease, only one third had
received training in oral health or instructions on how to
provide oral care. To complicate the matter more, dental

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coverage is curtailed under the Medicare and Medicaid


programs because the majority of dental services are
viewed as not medically necessary. Traditionally, Medicare
provides coverage for acute care only, which generally
does not include dental coverage. In the rare instances
where Medicare will provide dental coverage, the dental
procedure must be linked to an underlying health condition.
As a result, reimbursement for oral care under the Medicare and the Medicaid program is severely limited and
poorly funded.

Effectiveness of Oral Care Intervention Programs


The most compelling evidence obtained to date supporting
the effectiveness of oral care comes from several interventional studies that have demonstrated a reduction in
lower respiratory tract infections following improvement in
oral hygiene (Table 2).
Mechanical Intervention
In a randomized study of elderly nursing home patients,
Yoneyama et al. [42] randomized 417 patients to an oral
care group or no oral care group. In the oral care group,
nurses or caregivers cleaned the patients teeth with a
toothbrush for approximately 5 min after each meal. The
brushing was performed as usual daily tooth brushing,
including brushing palatal and mandibular mucosa and
tongue dorsum. If the toothbrush was not efficient, the
oropharynx was scrubbed with an applicator with povidone
iodine (1%). In the no oral care group, patients performed
tooth brushing by themselves irregularly. During a 2-year
follow-up, the incidence of pneumonia in the oral group
decreased from 19 to 11%. Mortality from pneumonia was
also about half that in patients not receiving oral care. The
study was criticized for lack of blinding, failure to adjust
for comorbidities, and the absence of a standard practice of
oral care in the control group. More significantly, the oral
care regimen implemented on those randomized to the
treatment arm was both too stringent and labor-intensive,
which made it impractical to be recommended as a standard of care for institutionalized subjects. In a similar
study, Adachi and coworkers [48] compared the effectiveness of weekly professional oral health care given by
dental hygienists to 77 residents of a long-term-care facility
compared to 64 residents who did not receive professional
oral health care. The prevalence of fevers of 37.8C or
more and the rate of fatal aspiration pneumonia in the
subjects receiving professional oral health care were significantly lower (4% and 5% vs. 7% and 16.7%, respectively; p \ 0.05). Of interest, 49 patients were not included
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

Yoneyama et al.
[42]

417 NH residents

Randomized controlled trial Daily tooth brushing plus


over 2-year period
scrubbing of pharynx with
povidone iodine 1% (including
professional care once a week)
vs. routine oral care

RR of developing pneumonia 1.67


in the group on no oral care
compared with oral care
(p = 0.04)

Simons et al. [59] 111 dentate elderly

Double-blind, randomized
controlled trial over
12-month period

CHX/xylitol gum vs. xylitol


(X) gum vs. no gum

Significant reduction in denture


debris, stomatitis, and cheilitis in
CHX/X and X groups compared
to no gum

Ueda et al. [49]

105 long-term-care
residents

Prospective interventional
study

Oral care intervention at intervals Oral hygienic condition could be


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
for 6 months

Weekly professional oral care


versus self oral care

Adachi et al. [62] 216 NH residents

Prospective interventional
study over 24 months

Ishikawa et al.
[63]

Prospective interventional
study over 5-month
period

Daily routine oral care plus either Fatal aspiration pneumonia


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
Professional oral care weekly vs. Professional oral care decreased
gargling with 0.35% povidone
burden of oropharyngeal bacteria
iodine daily vs. no professional
and was more effective than
care
gargling with povidone iodine

202 NH residents

Bassim et al. [29] 143 NH residents

Intervention

Outcomes

RR of developing influenza while


under professional oral care
compared to that in the control
group was 0.1 (95% CI 0.010.81, p = 0.008)

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


to determine the optimal frequency of professional intervention by dental health-care workers, Ueda et al. [49]
showed that oral hygienic condition could be improved by
performing professional oral care in which an interdental
toothbrush, an engine brush, and a scaler were used for
tooth cleaning at an interval of 1 week for 12 consecutive
weeks. The improved condition could be maintained when
professional oral care was continued at a 1-week interval
thereafter.
The benefit of oral care has also been shown to translate
into a reduction in influenza infection. Abe et al. [50]
assigned randomly 190 elderly patients to either professional oral care once a week or to self-care. The intervention
group had a significant drop in bacteria colony-forming
units (CFUs), NA, and TLPs compared to the control group,
and the rate of developing influenza was reduced by

tenfold in those assigned to professional oral cleaning


(p = 0.008).
A recent study involving 143 residents of a nursing
home investigated the association between the assignment
of an oral hygiene aide staff member and mortality from
pneumonia [29]. The oral care provided by the nursing
home oral hygiene aides included setting up for, encouraging, and monitoring self oral hygiene care for all residents who were aware and able to participate in their own
care. This included tooth brushing, antiseptic mouthwash
use, and oral and denture cleaning for edentulous or partially edentulous residents. For patients who were unable to
perform oral care, the aides would provide this care
directly. Looking at the records up to 79 weeks retrospectively, patients in the oral care group had significantly
lower plaque and debris scores (using the Simplified Oral
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


significant for mortality from pneumonia, the odds of dying
from pneumonia in the group that did not receive oral care
was more than three times that of the group that did receive
oral care (OR = 3.57, p = 0.03). However, the non-randomized controlled trial studies contributed to inconclusive
evidence on the association and correlation between oral
hygiene and pneumonia or respiratory tract infection in
elderly people.
Chemical Intervention
It is not always possible for disabled nursing home residents to brush their teeth or their dentures effectively,
hence chemical solutions for removing plaques and disinfecting acrylic resin became an alternative for mechanical
oral care in this population. Among these agents, chlorhexidine appeared on the market in mid-1970 s for use by
individuals undergoing periodontal treatment and dental
implant surgery. Chlorhexidine has bactericidal, fungicidal,
and some virus-killing properties. When used topically, the
N-chlorinated derivative of chlorhexidine binds covalently
to proteins in the skin and mucosa and results in a persistent antimicrobial effect with limited systemic absorption,
even after an oral ingestion. Compared to other antiseptics,
chlorhexidine is superior to Listerine and Meridol in its
ability to maintain low plaque scores and gingival health
during a 3-week period of no mechanical oral hygiene [51,
52]. Although decreased susceptibility to chlorhexidine has
been reported, it has not been convincingly shown to be
associated with repeated exposure to chlorhexidine [53].
Oral ingestion of chlorhexidine is usually well tolerated
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
data on chlorhexidine from nursing homes is scarcer and
definite evidence is still lacking. Nonetheless, Simons et al.
[59] described significant improvement in the stomatological health of nursing home residents following the mastication of chlorhexidine-containing chewing gum twice
daily for 12 months compared that of residents who chewed
a nonchlorhexidine-containing gum and that of a group that
did not chew gum. There were also increased salivary flow
rates, stabilized Streptococcus mutans and Lactobacilli
counts, and decreased prevalence of angular cheilitis, denture stomatitis, and denture debris. However, the study did
not assess the rate of respiratory infections in the treatment
arm nor in the placebo arm. More recently, Watando and
coworkers [60] investigated the effects of intensive oral
hygiene measures such as dental prophylaxis and chlorhexidine rinses on impaired cough reflex sensitivity, which is
a known risk factor for pneumonia. The results of the study

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showed that cough reflex sensitivity at 30 days in those with


intensive oral hygiene measures (intervention) was significantly higher than in the control (no intervention) group.
The odds ratio for improvement of cough reflex was 5.3 in
the intervention group compared with the control group;
however, no significant effect was seen with respect to
serum substance P, cognitive function, and activities of
daily living. The authors concluded that intensive oral
hygiene measures might reduce the incidence of pneumonia
by improving cough reflex sensitivity in the elderly. However, pneumonia was not included among the end points.
Nonetheless, the result of this study supports the need for
oral health-care interventions and indicates that improved
oral care may reduce the incidence of pneumonia.

Conclusion
The current review finds strong support for the need to
implement a program that uses oral hygiene in the longterm-care setting as part of daily routine. With skyrocketing
health-care costs and the increasing incidence of aspiration
pneumonia in the aging population, dental hygiene represents an effective cost-saving intervention. Programs to
improve oral health-care knowledge and skills, delivered by
dental professionals, must be included in the curricula of all
nurse-training establishments. In addition, programs for
practical training of care assistants in basic oral health care
need to be actively promoted in nursing homes. There is
also an urgent need for randomized controlled studies to
determine the optimal regimen(s) of an oral hygiene program in the prevention of NHAP [61].

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