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TYPE Review
PUBLISHED 04 June 2024
DOI 10.3389/fresc.2024.1337920

Impaired oral health: a required

companion of bacterial aspiration
EDITED BY
Phyllis Palmer,
University of New Mexico, United States
pneumonia
REVIEWED BY
Pamela Smith,
John R. Ashford*
Ohio University, United States SA Swallowing Services, Nashville, TN, United States
Rebecca Affoo,
Dalhousie University, Canada

*CORRESPONDENCE Laryngotracheal aspiration has a widely-held reputation as a primary cause of

John R. Ashford lower respiratory infections, such as pneumonia, and is a major concern of
[email protected]
care providers of the seriously ill orelderly frail patient. Laryngeal mechanical
RECEIVED 13 November 2023 inefficiency resulting in aspiration into the lower respiratory tract, by itself, is
ACCEPTED 20 May 2024
not the cause of pneumonia. It is but one of several factors that must be
PUBLISHED 04 June 2024
present simultaneously for pneumonia to develop. Aspiration of oral and
CITATION
gastric contentsoccurs often in healthy people of all ages and without
Ashford JR (2024) Impaired oral health: a
required companion of bacterial aspiration
significant pulmonary consequences. Inthe seriously ill or elderly frail
pneumonia. patient, higher concentrations of pathogens in the contents of theaspirate
Front. Rehabil. Sci. 5:1337920. are the primary catalyst for pulmonary infection development if in an
doi: 10.3389/fresc.2024.1337920 immunocompromised lower respiratory system. The oral cavity is a complex
COPYRIGHT and ever changing eco-environment striving to maintain homogeneity
© 2024 Ashford. This is an open-access article among the numerous microbial communities inhabiting its surfaces. Poor
distributed under the terms of the Creative
Commons Attribution License (CC BY). The maintenance of these surfaces to prevent infection can result inpathogenic
use, distribution or reproduction in other changes to these microbial communities and, with subsequent proliferation,
forums is permitted, provided the original can altermicrobial communities in the tracheal and bronchial passages. Higher
author(s) and the copyright owner(s) are
credited and that the original publication in bacterial pathogen concentrations mixing with oral secretions, or with foods,
this journal is cited, in accordance with when aspirated into an immunecompromised lower respiratory complex, may
accepted academic practice. No use, result in bacterial aspiration pneumonia development, or other respiratory or
distribution or reproduction is permitted
which does not comply with these terms. systemic diseases. A large volume of clinical evidence makes it clear that oral
cleaning regimens, when used in caring for ill or frail patients in hospitals and
long-term care facilities, drastically reduce the incidence of respiratory
infection and death. The purpose of this narrative review is to examine oral
health as a required causative companionin bacterial aspiration pneumonia
development, and the effectiveness of oral infection control inthe prevention
of this disease.

KEYWORDS

oral hygiene, pneumonia, aspiration, microbial communities, bacterial aspiration

pneumonia, aspiration pneumonia, oral infection control, oral care

1 Introduction
Aspiration is one of the contributing causes of many lung diseases, including acute
respiratory distress syndrome, aspiration bronchiolitis, aspiration pneumonia, aspiration
pneumonitis, exogenous lipoid pneumonia, interstitial fibrosis, bronchiectasis, chronic
obstructive pulmonary disease, and asthma (1–4). Bacterial aspiration pneumonia
(BAP) (5–7) accounts for 5% to 24% of all types of pneumonia (8), ranks eighth among
all causes of death, and is first among infectious diseases causing death (9). Aspiration
can be broken down into two components: a pathophysiological event and the aspirate
content. Motor/sensory impairment of the larynx is, in and of itself, not the cause of

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these diseases (10). Larynx closure incompetency due to disease is present simultaneously for BAP to develop (18–20). Reducing or
but an exacerbation of an otherwise normal conveyance of eliminating the effects of any one of these three factors through
secretions from the oral cavity into the lower respiratory system. focused treatment significantly reduces the likelihood of BAP
The source, content, and volume of the aspirate cause disease. developing. The purpose of this narrative review is to examine
Efforts to define aspiration pneumonia have been illusory and one of these foundational, but complex factors, the presence of
lacking in completeness and specificity (11). Mandell and acute oral disease, and its role in BAP development. This review
Niederman (12) define it as an infection caused by specific will examine the structures and ecology of the oral cavity, its
microorganisms, while Marik (13) describes it as an infectious defenses, its disease contributions to illness, and the effectiveness
process caused by inhalation of oropharyngeal secretions that are of oral infection control in the prevention of bacterial-based
colonized by pathogenic bacteria. Ferguson and colleagues (14) aspiration pneumonia.
contend that use of the term, aspiration pneumonia, is
ambiguous and may lead to confusion of the pathogenesis and
treatment. They propose using the term, accidental foreign body 2 Normal oral environment—structure
aspiration, mainly focusing on objects aspirated, such as coins, and ecology
teeth, nuts, metal objects, and similar materials. Further, the
Japanese Respiratory Society (15) adopted a more specific 2.1 Oral Mucosa
diagnostic definition based on clinical parameters including
infiltrates on chest radiographs, suspected or direct confirmation For the oral cavity to remain healthy, the oral mucosa, oral
of aspiration, and elevated peripheral white blood cell count. secretions, teeth properties, and the oral microbiota must work
Other factors may include the content and volume of the in concert to maintain environmental homeostasis. The oral
aspirated material, the frequency of aspiration events, and the epithelium is an environmentally protective barrier to the tissues
host’s response to the aspirated material (16). deep to its surface (21–23) (see Figure 2). Squamous epithelium
Immune dysregulation, swallowing impairment, recurrent is a soft tissue membrane of three-layered divisions: the surface
infections, multiple comorbidities, and poor prognosis go well oral epithelium composed of stratified squamous epithelium, an
beyond ineffective airway clearing and are common factors found underlying layer of connective tissue or the lamina propria, and
in patients with stroke-associated pneumonia or frailty-associated the deepest layer composed of dense irregular connective tissue,
pneumonia (17). To encompass these factors into a clinically- or the submucosa (22). This epithelial structure, which is
useable model is challenging. A three-factor model is proposed comprised of close to 40 structurally overlapping squamous cell
that prompts equal clinical consideration of the three primary layers, cellular cornification, and cell interactions, serves as a
underlying conditions that must be present simultaneously for protective barrier against external forces. There are roughly
BAP to develop: (1) the presence of a serious illness or frailty 1.540 × 107 superficial or exposed epithelial cells in the mouth
with associated compromised immune functions; (2) the presence (23). Three types of squamous epithelium cover the oral cavity
of acute oral disease; and (3) the presence of impaired surfaces and differ in histology and function. The lining mucosa
sensorimotor functions of the airway protective mechanism. This
model is called the Three Pillars of Bacterial Aspiration
Pneumonia (see Figure 1) and defines the three underlying
foundational conditions necessary for bacterial aspiration
pneumonia to develop. These three factors, or pillars, must be

FIGURE 1 FIGURE 2
Three pillars of bacterial aspiration pneumonia. Squamous cell epithelium.

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is a thin and non-keratinized (elastic or flexible) tissue comprising rates than women (23, 26). A healthy person’s glands produce
the surfaces of the cheeks, lips, soft palate, alveolar mucosa, floor of roughly 600 ml of saliva per day with the highest flow rates in
the mouth, and vestibular fornix (21, 22). The masticatory mucosa the afternoon and decreasing during sleep (34). The average oral
is a tough epithelium varying in thickness and tightly attaching to volume of saliva in the mouth for men before swallowing is
hard surfaces such as the hard palate and the base of the teeth. 1.1 ml, and after swallowing, 0.8 ml. These volumes are slightly
This tight, adhesive mucosa contains keratin and is more resilient less for women. Thus, with each normal saliva swallowing event,
and resists deformity by forces generated during mastication about 0.3 ml is removed from the oral cavity into the airway/
(22, 24, 25). With inflammation and tissue breakdown, it digestive structures below (30, 35). Comprised of over 2,000
becomes a prime site for infection development and for proteins, peptides, and inorganic compounds (36, 37), some of
pathogens to colonize. The tongue mucosa, sometimes classified these proteins provide immune properties such as fibronectin,
as masticatory mucosa, is a special keratinized squamous immunoglobulins, defensins, lactoferrin and glycoproteins (38).
epithelium with unique properties including lingual papillae and Immunoglobulin A (IgA) is an antibody secreted by plasma cells
taste buds (24). The dorsum of the tongue plays an active and in the salivary glands producing secretory IgA (SIgA). SIgA
crucial role in mastication (22). It’s cornified structure, while functions to bind with bacteria preventing them from reaching
structurally resistive, allows oral microbes and debris to collect the oral epithelium (39). While saliva is a poor source of
on its surface and provides a location for pathogens to thrive. nutrition for bacteria, one ml can contain up to 108 colony
The surface areas of the normal oral mucosa are sloughed and forming bacterial units. The constant movement and agitation of
replaced about every 2.7 h, which prevents bacteria from saliva works to wash and remove shedding squamous cell
attaching permanently. With 40 layers of epithelium, 4.5 days are surfaces and reduces the potential for bacteria attachment (40).
required to completely regenerate the oral mucosa (23). Dehydration, one of the most common electrolyte disorders
among elderly patients, and a primary reason for hospital
admission, may directly affect saliva flow (41). As a result, saliva
2.2 Oral secretions flow rates are reduced, or hyposalivation, increasing saliva
protein concentrations and osmolality (42). Fortes and colleagues
The importance of oral secretions, their functions, and (43) report that induced exercise dehydration decreased
contributions to help maintain normal health cannot be unstimulated saliva flow rate and increased the concentration of
understated. Saliva provides the primary watery mechanical and SIgA, thus decreasing mucosal immunity protection. Lack of
chemical protective covering over all oral surfaces and plays a adequate saliva flow movement and agitation may contribute to
critical role in oral homeostasis and tissue repair (22, 26, 27). the development of oral mucositis and increase oropharyngeal
The surfaces of the oral cavity normally remain wet from colonization with gram-negative bacteria (44). Saliva production
continuously unstimulated secreted glandular fluid (28). Three and flow decreases are gland-specific and associated with the
pairs of glands–parotid, submandibular, and sublingual–secrete aging process (45), radiation therapy effects (46), and with the
90% of the saliva (29). The submandibular and sublingual glands side effects from over 400 medications (47). With aging, low
provide close to 75% of unstimulated saliva containing mucins. salivary flow rates increase the susceptibility to dental caries due
Mucins form a slimy lubricating coating over surfaces to prevent to low buffering capacity of saliva and reduced clearance of oral
insults to the tissues during eating (30). Clusters of minor food debris from tooth surfaces (48, 49). This further increases
salivary glands are dispersed throughout the buccal, labial, distal the risks for oral infection, periodontal disease, and tooth loss
palatal, and lingual cavity regions and secrete the remaining 10% (50). Hyposalivation elevates the risks of health complications
of the saliva. These glands generally function continuously and affecting the older patient’s quality of life such as altering dietary
secrete mucous with some thinner sero-mucous fluid (28, 31). practices, nutritional status, taste, speech, and use of dental
Saliva has many functions beyond maintaining oral wetness appliances. Jwabuchi et al. (51) followed over 278 dental patients
and these are listed in Table 1. The average saliva flow rate for over the age of 40 for six months to determine the incidence of
healthy adults is about 0.3 ml/min with younger adults having a lower respiratory infections. Sixty percent reported acute
higher flow rate than older adults, and men having higher flow respiratory infections over the period with 96 subjects (35%)
reporting hyposalivation. Aging, however, does not appear to
affect parotid and minor gland saliva flow, which is integral to
TABLE 1 Functions of Saliva (32, 33). biofilm formation on tooth enamel, acid neutralization, oral
rinsing, and digestion (52). Restoring salivary flow, as a
Functions of saliva
treatment including adequate water intake, may assist in
1. Dilutes substances to stimulate taste receptors.
2. Dilutes harmful sugars.
returning the oral cavity to a healthy homeostatic environment
3. Cleanses oral cavities of bacteria and food residues reducing pathogenic biofilm formation and the potential for
4. Lubricates surfaces with mucins to control bacterial and fungal colonization. infection development.
5. Buffers or neutralizes acidogenic microorganism that cause tooth decay. Alternative feeding avenues may also impact salivary flow rates
6. Promotes remineralization of tooth enamel. and saliva composition. Leibovitz and colleagues (53) examined 23
7. Facilitates the oral preparatory stage of swallowing.
elderly residents in long-term care facilities using prolonged
8. Initiates digestion
nasogastric tube feeding (NGT). Compared to a control group,

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the NGT residents showed alterations in enzyme, elementals, and (64, 65). The periodontium is connective tissue consisting of the
minerals in saliva composition and a significantly higher rate of cementum, the periodontal ligament, alveolar bone and gingival
oral pathogen colonization. Prolonged nasogastric tube feeding tissue (66). These area locations along the alveolar ridges are
was associated with pathologic oropharynx colonization primarily where dental disease characteristically develops and
associated with saliva alterations and related to increased risk for becomes the focus of disease prevention.
pneumonia from aspiration. Kim and Han (54) examined the
salivary flow rates of post-CVA patients and found their flow
rates were significantly lower than those of healthy subjects. 2.4 Oral microbiome
However, they could not rule out potential effects of medications
taken by the stroke group. The human oral cavity contains over 700 species of bacteria
Sebaceous glands primarily located close to and surrounding identified through 16S rRNA sequencing phylogeny (67). Most
the mouth in the lips, labial, and buccal mucosa secrete small species are commensal bacteria, or indigenous flora, co-
amounts of sebum, a sticky, oily substance. The functions of inhabiting on the mucosal and dental surfaces through biofilm
these oral sebaceous glands have not been clearly determined development. Chief among the pioneer colonizers are commensal
(22). However, Hoover et al. (55) reported that sebum seals in streptococci. This bacteria species is multi-faceted. Some cause
moisture in deeper cellular levels, promotes lubrication, protects enamel demineralization resulting in cavities. Some support other
against environmental and infectious insults, and provides pathogens in periodontitis development. Others interfere with or
immunity functions. prevent colonization of tooth surfaces, and still others help
The final oral secretion is gingival crevicular fluid (GCF). It is modulate the host immune response (68). Immediately after
an exudate released into the gingival sulcus by increased tooth brushing, these pioneer colonizers, or gram-positive
permeability of the capillaries in the gingival tissues in response bacteria, attach to the tooth surfaces in parallel arrays and extend
to inflammation. In the healthy oral environment, these outward. Secondary and tertiary commensal colonizers attach to
capillaries produce very small amounts of GCF as a serum to these arrays forming biofilms (more later). Most of the oral
flush the gingival sulcus of pathogens and toxic matter and to microbes are commensal, while a few are opportunists with the
cushion the tooth against insult (56). Inflammatory immune potential to become pathogenic under certain conditions, or
cells, primarily neutrophils, are present in the dense capillary pathobionts (69). By alerting the host immune system to
concentration in the basement membrane and epithelium and invading oral pathogens, commensal bacteria work to maintain a
help to maintain the health of the gingiva sulcus and fight communal homogeneity among the many species of microbes
inflammation. The output flow of GCF maximizes to bathe the (70). The total number of bacteria in the healthy mouth at any
area affected by trauma and gingiva inflammation from one time will depend on (1) the number attached to the
mastication of course food, dental pocket depth, intracrevicular superficial epithelial cells of the mucosa, (2) the number free
scraping, scaling, and histamine, and topical application. More floating in saliva, (3) the number attached to epithelial cells
recently, GCF analyses have identified protein biomarkers that floating in saliva, (4) the number in periodontal pockets, and (5)
may reflect early periodontal disease development, as a precursor the number attached to teeth (23). As previously stated, there are
to potential respiratory infection, and its progression (57, 58). 1.54 × 107 surface epithelial cells exposed in the mouth. Dawes
(23) calculated there are approximately 100 bacteria attached to
each epithelial cell, or 1.54 × 109 in total. These flora form
2.3 Teeth into biofilm communities and colonize different sites in the
oral cavity (71). Segata and colleagues (72) identified three
Hard enamel, or carbonated phosphate, composes the structure community groups with distinct bacteria taxonomy: Group 1,
of teeth and is the only substance that does not regenerate through buccal mucosa, keratinized gingiva, and hard palate, which
metabolism (59–61). Heavy concentrations of hair keratins in the harbor a low microbial density; Group 2, saliva, tongue, tonsils,
enamel resist decay but allow the attachment of biofilms (62). and back wall of oropharynx supporting higher microbial density
Enamel covers the crown of the tooth and depends on a delicate with the papillated tongue mucosa supporting a highest
balancing process of demineralization and remineralization to microbial density; and Group 3, sub-and supra-gingival plaque
remain healthy. Remineralization occurs with saliva delivering on tooth surfaces. The non-shedding teeth surfaces accumulate
calcium, phosphate, and fluoride to the surfaces, and from oral significantly more microbes embedded in dental plaque
cleaning with fluoride toothpastes. Demineralization of the (73). These attached bacteria can reach more than 1011
enamel and the underlying dentine results from dietary food microorganisms per milligram of dental plaque (74).
acids and lactic acids produced by anaerobic, gram-positive Bacteria dispersal within the oral cavity, both actively and
bacteria, such as Streptococcus mutans, Streptococcus sobrinum, passively, determines the overall oral bacteria load present in the
and lactobacilli (63). Resulting enamel cavities harbor beds of cavity at any one time. Active bacterial dispersal occurs through
pathogens linked to lower respiratory infections. Cellular or surface erosion, sloughing, and reseeding in spaces on and within
acellular cementum binding covers the root of the tooth, which the biofilm covering the tooth surfaces. Passive dispersal is from
supports the crown. The root is embedded in the periodontal salivary flow forces generated across oral surfaces, surface space
socket in the alveolar bones of the mandible and maxilla competition among bacteria, and dislodging through mechanical

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forces from teeth occlusion and food mastication (75–77). The sterility, and the conceptual errors that have supported this
number of bacteria floating unattached in saliva accounts for premise. Modern approaches to studying the lower respiratory
approximately 3.68 × 106 (27.7%) of the total oral bacterial count, system microbiome, and without contamination, include
while bacteria attached to sloughed squamous cells floating in collecting the 16S rRNA gene from a bacterial genome and
saliva account for 9.59 × 106 (72.3%), or a total of 13.27 × 106 sequencing its single specimens of DNA. Dickson and his group
bacteria suspended in saliva. Thus, most saliva-suspended (85), using this method, proposed an adaptive island model of
bacteria are attached to sloughed epithelial cells (23). As noted lung biogeography. In the healthy person, the ecosystem is a
earlier, most adults swallow approximately 0.3 ml of saliva per constant and dynamic migration of microbes via microaspiration
swallow event. With a total bacterium count of 13.27 × 106 from the nasopharynx and oropharynx into the lower respiratory
suspended in saliva, Dawes (23) estimates the bacteria load per system. This migration supports commensal microbe
swallow of saliva to be 3.619090 × 106 for the orally healthy communities in the lower respiratory system like those found in
person, or about 27.3% of the total bacteria load in saliva at the the oral cavity. In a later paper, Dickson and associates (86)
time of the swallow. Bacteria growth doubling in dental biofilms reported the greatest community densities are located at the
varies from 3 to 14 h depending on the number of layers. carina and proximal bronchus intermedius, which coincides with
Oyetola and colleagues (78) report salivary bacteria loads are gravity-associated microaspiration flow along the right bronchus.
significantly higher for subjects with periodontitis compared to The environmental balance of these lower respiratory microbial
those without periodontitis. Using colony counting, they reported populations and their densities are maintained through
the salivary bacteria count was highest among those with communal immigration, elimination, and reproduction (83).
poor oral hygiene (1.89 × 108 per ml). A bacteria load of Evidence strongly supports the direct connection of bacterial
this magnitude in saliva and when aspirated into an communities through mouth-lung immigration with the
immunocompromised lower respiratory system increases the risk abundance of similar microbes identified in oral and lung
of developing bacterial aspiration pneumonia (10, 79, 80). specimens, including Prevotella sp. and Veillonella sp (86).
Berger and colleagues (81) report that environmental factors, Ecological homeostasis of these similar commensal communities
diet of individuals, microbial migrations, and genetic factors in the mouth and lungs can abruptly change with the onset of
contribute to the diversity and balance of the oral microbial serious illness and accompanying immunocompromise. These
communities. Opportunistic pathobiontic microbes may turn changes result in highly virulent bacterial biomasses reducing
pathogenic, or foreign pathogens may invade when the host community diversities. Through oropharyngeal migration via
becomes susceptible through immunodeficiency, pathogen microaspiration of these pathogens into the lower respiratory
infection, and treatment with antibiotics and other drugs (82). system, commensal bacterial communities already present in the
Maintaining homogeneity among the commensal bacterial bronchi become dysbiotic (86–90). The most frequently cultured
communities is a complex operation involving the host immune bacteria in patients with aspiration pneumonia and commonly
system as these microbes’ struggle to compete and survive in an found in the oral cavity are gram-negative rods, such as
ever-changing environment. How a healthy microbiome evolves Escherichia coli, Klebsiella pneumoniae, Staphylococcus aureus,
into a pathobiome is not well understood. Sultan and colleagues and Pseudomonas aeruginosa (12, 14, 91). This pathogen-
(72) describe it as commensal microbes breaching the barrier of dominated imbalance promotes inflammation and subsequent
commensals becoming pathogenic. This transition results in an development of respiratory infections, such as BAP (86, 87).
overgrowth or imbalance of opportunistic, proinflammatory
pathogens disrupting the oral ecosystem balance, or dysbiosis.
Oral diseases develop “as a result of a change in the 2.5 Oral biofilm
proportion of certain species with greater pathogenic potential
within the indigenous flora” (p.4). For an excellent review of Biofilms form in natural and industrial systems. Earlier, it was
the intricacies of the immune system policing the oral discussed that parallel arrays of layers of slow-growing, commensal
environment, see Sultan et al. (73). bacteria embedded in a gummy glycoprotein and glycolipid
Medical science has taught without cited evidence or argument (glycocalyx) exudate attach to surfaces, such as the teeth, to form
the concept that the lung environment is sterile (83). Cursory biofilms (69, 91, 92). Sauer and colleagues (93) describe the
understanding of basic human anatomy confirms the airway is stages of biofilm development for the bacteria, Pseudomonas
constantly open to the outside environment allowing the influx aeruginosa, and these stages are graphicly depicted in Figure 3.
of thousands of particles, bacteria, fungi, and viruses inhaled Bacteria encased in biofilm exudate communicate with each
daily. Under these circumstances, the immune response cannot other through molecular diffusion called quorum sensing. This
reasonably maintain a sterile environment. Hilty and colleagues signaling ability benefits the bacteria with host colonization,
(84) were among the first to challenge the lung sterility belief biofilm formation, defense against invader microbes, and
after culturing samples taken from patients with asthma and adaptation to oral environmental changes. Additionally, quorum-
COPD and comparing them to normal controls. They identified sensing also enables some pathogens to tolerate host defenses
similar flora in the bronchial tree among all the subjects with and antimicrobial treatments (94).
asthma, COPD or who were normal. Dickson and associates (83) Dental plaque is an oral biofilm visible around the gingival
provide an excellent review of the origins of the notion of lung surfaces of the teeth (95). The teeth, not having the shedding

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FIGURE 3
Stages of biofilm development (93).

protective properties of the mucosa, are better attachment surfaces over, over 96% have dental caries. The number of decayed teeth
for bacteria and dental plaque (79, 90). Saxon, as reported by was a significant predictor (p < 0.01) of pneumonia among 189
Rowshani and colleagues (96), states that bacteria begin to elderly long-term care residents in a study by Langmore and
recolonize and form new biofilms within three hours of cleaning associates (10). In a follow-up study of 358 subjects, Terpenning
when adjacent to healthy gingiva. This agrees with Dawes’ and colleagues (105) identified significant risk factors for BAP to
findings discussed earlier (23). However, if the gingiva becomes include the number of functional dental units, and the number
inflamed, bacteria recolonization can return within 5 min of of decayed teeth, Streptococcus sobrinus and Staphylococcus
cleaning. Bacteria housed and protected in plaque initiate aureus in saliva and periodontal disease, and Porphyromonous
processes responsible for dental caries and periodontal disease gingivalis in dental plaque.
discussed earlier. Abdulkareem and associates (77) provide
excellent descriptions of the complex processes of biofilm
formation and development in the oral cavity. 3.2 Periodontal disease—local and
system-associated diseases

3 Oral care-associated diseases Periodontal disease is a significant risk factor for BAP (106).
This inclusive term is used to describe a group of different
3.1 Dental caries—local disease biologic conditions causing localized inflammatory disease in the
periodontal tissues (74). Assays of oral cavities with periodontal
Tooth decay is a biofilm-mediated, multifactorial, localized disease, particularly periodontitis, reveal the presence of gram-
disease and one of the most common preventable diseases across negative bacteria, such as Porphyromonas gingivalis, Bacteroides
the lifespan (97, 98). As discussed earlier, Streptococcus mutans forsythus, and Actinobacillus actinomycetemcomitans (107). This
(S mutans), a common gram-positive bacterium, and various disease results from poor oral health maintenance to remove
lactobacilli bacterial species found in the plaque on teeth surfaces proinflammatory bacterial-encrusted plaque. These pathogenic
cause tooth decay. Person-to-person contact introduces microbes bacterial communities release by-products that induce
to others, such as a mother or care giver to a new baby. Tooth inflammation of the gums and eventual destruction of the bone
decay is caused when these pathogens digest sugar forming lactic supporting the teeth (108, 109). For adults 30 years and older,
acids. These acids deplete calcium phosphate in the tooth four out of 10 have periodontal disease. Worldwide, 20%–50% of
eroding and penetrating the enamel structure (99, 100). The the population has periodontal disease (110, 111).
enamel surface weakens and collapses forming a cavity from With the initial onset of periodontal inflammation, the
demineralization (101, 102). Pathogens may also enter the microbial communities become pathobiomes (77, 94, 112, 113).
bloodstream following dental procedures, or from daily dental Kinane (108) reports that these communities may be populated
hygiene practices. Vascular inflammation from these pathogens by fewer than 10–20 pathogen species and may initiate the onset
may result in systemic diseases such as infective endocarditis or of periodontal disease within 10 days if the oral environment is
may promote tumor metastasis (80). While some studies have poorly cared for. Kinane (108) provides an excellent discussion
not directly linked S mutans to aspiration pneumonia, Loesche of the host-based risk factors for periodontal disease progression.
(103) has linked S mutans to tooth decay. In a report by Dye Table 2 list some of these factors.
et al. (104), approximately 91% of adults aged 20 to 64 years Pathogen-laden biofilms covering the teeth and gingiva evolve
have dental caries and 27% are untreated. In the 65 years and and become more attracted to and persist in the inflamed tissue

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TABLE 2 Host-based risk factors for periodontal disease progression Treponema (117). If left untreated, gingivitis can potentially
(108).
progress to periodontitis within 6 months in some individuals
Periodontal disease risk factors (118). Better understanding of this progressive inflammatory
Aging processes process has evolved since the 1960’s with evidence placing the
Poor oral hygiene focus on bacterial-laden biofilms as a leading factor in
Salivary gland dysfunction periodontal disease development. Subsequently, in a landmark
Dietary habits
paper, Page and Schroeder (119) describe a four-stage model for
Smoking
the progressive pathogenesis of this disease based upon the
Gingival inflammation
Hormonal changes body’s immune response. This model describes the progressive
Socioeconomic status influx of the innate immune phagocytes, i.e., neutrophils,
Race responding to the initial stage of inflammation and progressing
Medications to the adaptive system’s antibody-producing plasma cells
Genetic influences responding in the advanced stages of the disease. This model, for
Systemic diseases
the first time, provides a foundation for understanding the
Stress, distress and coping behaviors
pathogenesis of periodontal disease. Later models have expanded
the Page and Schroder model to help explain the persistence of
disease development and to better understand the cellular and
environment. These pathogens are protective and self-sustaining by molecular mechanisms underlying functions of immune and
developing defenses against immune responses and establishing inflammatory responses (120).
sources of nutrition. Thus, with increasing inflammation of the Periodontitis is a low-grade, chronic inflammatory systemic
gingiva, pathogen-laden communities increase their biomasses disease that progresses from gingivitis to destroying the
(114). The most recent model by Van Dyke and his group (115) periodontium (gingiva, periodontal ligament, and alveolar
provides a holistic view of how gingival inflammation is the bone) supporting the teeth in the gingival sulcus (121). A
primary source of plaque-associated periodontal disease. This self-perpetuating positive feedback loop forms as the
model describes a 5-stage progression for disease development proinflammatory and immune deregulated dysbiotic microbiota
beginning with healthy gingiva to severe periodontitis and is in the oral cavity foster destructive inflammation. The resulting
shown graphically in Figure 4. inflammation provides a nutritional source for periodontitis-
Gingivitis, the most common and earliest stage of periodontal related pathogens, increasing their growth potential (122). The
disease, develops as a local inflammatory response around the base proximity of these oral pathogens to the bloodstream circulating
of the teeth and in the gingival sulcus. This response is limited to in the gingiva and gingival sulcus can cause bacterial by-products
the soft gingival epithelium and connective tissue (116). Microbiota to spread throughout the body, further producing remote acute
assayed at the infected gingiva includes species of gram-negative and chronic inflammation. Numerous studies (123–125) link
Streptococcus, Fusobacterium, Actinomyces, Veillonella, and chronic inflammatory periodontal disease with over 100 systemic

FIGURE 4
The five stages of periodontal disease (115).

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TABLE 3 Systemic diseases linked to periodontal disease (74, 121, 122, an immuno-compromised and inflamed lower respiratory system.
126–128).
The result is respiratory disease development, such as BAP.
Systemic diseases
Atherosclerosis Bacterial pneumonia
Diabetes Chronic obstructive pulmonary disease
Rheumatoid arthritis Alzheimer disease
4 Oral hygiene care
Preeclampsia Nonalcoholic fatty liver disease
Preterm birth Colorectal cancer 4.1 Oral hygiene cleaning and rinses
Inflammatory bowel disease Chronic kidney disease
Myocardial infarction Peripheral vascular disease 4.1.1 Toothbrushing
Stroke Coronary heart disease The toothbrush is the primary tool for cleaning the oral cavity
Infective endocarditis Obesity (136). The American Dental Association recommends brushing the
Metabolic disorders Oral cancer
teeth twice daily with fluoride toothpaste for two minutes at a 45o
Pancreatic cancer Esophageal cancer
angle to clean the crown and the gingiva (137, 138) see Figure 5A.
Emphysema
Most populations do not clean their teeth thoroughly enough
to adequately control or prevent dental plaque growth (136).
Further, a recognized standard technique does not exist for
diseases. Table 3 lists some of these periodontitis-related manually cleaning the teeth and other oral surfaces when caring
systemic diseases. for people in hospitals or nursing care homes. However, the
Evidence that periodontal disease is a primary causative factor primary purpose remains the same—removal of bacterial plaque
in BAP development is strong (106, 129–135). Cultures from to prevent oral infection–and a bristled brush remains the
patients with BAP have identified respiratory pathogens including primary tool. Buglass (139) reports that the primary purposes of
Porphyromonas gingivalis, Aggregatibacter actinomycetemomitans, oral hygiene care are (1) to maintain a functional and
Peptostreptococcus, Bacteroides, Prevotella, Fusobacteria, comfortable oral cavity, (2) to enhance self-esteem, and (3) to
Streptococcus pneumoniae, Hemophilus influenzae, Staphylococcus reduce bacteria activity in the mouth reducing the potential risk
aureus, and Enterobacteriaceae (133). This connection of of local and systemic infection. Clinical evidence supports the
pathogens identified in the dysbiotic communities of the oral premise that regular oral cleaning reduces oral bacteria and
cavity with those found in the lower respiratory system in significantly reduces the incidence of BAP (88, 137, 139–144).
patients with pneumonia strongly supports the Three Pillars With ICU ventilator patients, the number of brushings per day
model advanced earlier. Each pillar is linked by underlying may vary from two (145, 146), three (146–149), or four (150). de
inflammatory processes. Pathogenic biofilms only develop in Lacerda and associates (151), in a prospective, randomized study
immune compromised inflammatory conditions in the oral cavity. of 716 ICU patients, report that toothbrushing is associated with
Pathogens from these biofilms subsequently migrate via saliva- a significant reduction in the length of time on the mechanical
laden microaspiration or food-laden macroaspiration through an ventilator. The incidence of ventilator-associated pneumonia
inflammatory-induced, mechanically-inefficient larynx and into (v-BAP) and length of ICU stay were also reduced but without

FIGURE 5
Toothbrushing and toothette cleaning. (A) Brushing removes plaque. (B) Toothette sponges do not remove plaque.

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statistical significance. Alhazzani and colleagues (150) report weeks, they reported no significant differences between the two
similar findings from a systematic review of six studies of 1,408 groups, but both groups showed a reduction in gingiva bleeding.
patients. Thus, regular toothbrushing with ICU patients may Reduction in gingiva bleeding and inflammation is also reported
reduce time on ventilation but has smaller effects on reducing by Wang (164). Others (165, 166) report modest to no
the incidence of pneumonia. Nursing care home residents receive significant differences in dental plaque scores between electric
toothbrushing less often and less consistently than is and manual toothbrushes use by long-term care residents. One
recommended by the American Dental Association. Hopcraft’s advantage to using power toothbrushes with the elderly is that
group (152) surveyed 275 Australian long-term care residents they do not require special dexterity as do manual toothbrushes.
and examined the periodontal health of each. Less than one-third The powered toothbrush is easier to use with this population and
of the residents reported brushing their teeth twice or more is an excellent alternative to manual toothbrushing (167).
daily. Less than one-half reported cleaning their teeth only once
a day. For residents requiring assistance with oral hygiene from 4.1.2 Toothette sponges and swabs
the nursing staff, the frequency and consistency of toothbrushing Nursing staffs commonly use lemon glycerin swabs and foam
was very low. Residents with dementia demonstrated poorer oral sponges, or toothettes, for oral cleaning instead of soft
hygiene than those without dementia, however, the differences toothbrushes, particularly with difficult patients or intubated
were not significant. Overall, periodontal health was extremely patients. Grap et al. (168) report that sponge toothettes do not
poor. Similar findings have also been reported (149, 153, 154). work effectively to remove dental plaque. Sponges are not
Hopcraft et al. (152) associated poor oral hygiene in nursing sufficiently abrasive to remove plaque, and cannot penetrate the
care homes with lack of assistance from staff with brushing, low gingival tissue around the base of the teeth for cleaning see
frequency of brushing, and periodontal disease. Islas-Granillo Figure 5B. Huang and colleagues (169) report findings on 282
and colleagues (155) report similar survey findings with adults patients using nasogastric tube feeding and receiving oral care
over 60 years living in long-term care facilities or living in the using an oral cleaning sponge only. Those receiving sponge oral
community. Fifty-three (53.2%) percent of respondents reported hygiene care had a 3.94 times higher rate of pneumonia than
brushing their teeth at least once a day. Younger and female those using toothbrush cleanings. Despite evidence that sponges
participants used oral cleaning aids, such as mouth rinses and are ineffective for plaque removal, they continue to be a primary
dental floss, more often than did older participants. Islas-Granillo tool for oral care (168). Sponges and lemon swabs should be
et al. further reported that self-dependent residents had better used only to clean the oral mucosal surfaces of excessive mucus
oral hygiene than dependent residents requiring staff assistance. collection and other debris from the mouth before toothbrush
Coleman and Watson (156) report only 16% of residents cleaning or applying liquid antiseptic to the oral surfaces (170).
received oral care from nursing assistants in their observational
study. Wagner et al. (157) telemonitored nursing assistants 4.1.3 Rinses
administering oral care over a 100-day period. The average Dentists encourage the practice of swishing liquid in the mouth
number of days a resident received one brushing per day was following eating. Swishing agitation generates pressure around the
24.45 days. The mean number of days a resident who did not teeth loosening and removing food particles from tooth crevasses
receive oral care at all was 40.38 out of 100. Three months after and rinsing sugars from surfaces. Ikeda et al. (171) report that
the researchers discontinued the monitoring program, the wiping the inside of the mouth with mouth wipes is as effective
residents lost any oral gains made during the monitored trials. as rinsing with water and suctioning. That mouth rinses can help
Similar results were reported by Gurgel-Juarez et al. (158) for control biofilm development leading to halitosis, gingivitis,
hospital stroke unit patients who received baths 4 times more plaque, and tooth decay is not a recent idea. August Wadsworth
frequently than oral care. Further, oral care was not documented (172), a distinguished scholar of Pathology at Columbia
during the patient’s hospitalization in over one-half of the cases. University at the first of the twentieth century, recognized that
There have been questions over whether the powered mouth secretions contained virulent bacteria species, both in
toothbrush is better than the manual toothbrush for removing healthy and diseased individuals. His objective was to destroy
plaque and preventing gingivitis. Using a Cochrane Database these pathogens to prevent pneumonia but discovered they
systematic review, Yaacob and associates (159), compared manual regenerated within hours. Antiseptic mouthwashes were in the
and powered toothbrushes in everyday use by people of any age early stages of development and he warned that these products
to determine the effectiveness of plaque removal, health of the should not only destroy the bacteria, but should also be non-
gingivae, staining, and calculus, among other areas. Reviewing abrasive to the oral mucosa, and safe, if swallowed. Early
findings of 4,624 participants from 51 trials, they determined experiments using potassium chlorate, lysol, formaldehyde,
that powered toothbrushes provide a significant benefit over hydrogen peroxide, and alcohol showed little to no effectiveness.
manual toothbrushing for reducing plaque and gingivitis with Of this list, alcohol continues to be used today in some rinses.
both short-term and long-term use. Several other studies support Mouth washes may be preventative or therapeutic. Preventative
these findings (160–162). Lavigne and colleagues (163), however, oral treatment is the long-term use of a product to control
used a single-blind model in a long-term care population to plaque buildup, and therapeutic use is short-termed to assist with
determine if the use of a rotary toothbrush reduced periodontal oral healing or before and after operative procedures (173). As
inflammation compared to usual manual brushing care. After six an antiseptic, the fluid can reach small areas around the teeth

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acting against the lipids and proteins composing the biofilm, and with which specific pathogen species are causing the pneumonia
penetrate to attack bacteria, reducing the bacteria load in the and which antiseptics are most effective against those specific
oral cavity (174). pathogens. Studies of mouthwashes using essential oils support
Mouth rinses are classified as cosmetic products and vary in their anti-plaque and anti-gingivitis effectiveness (199, 200).
their chemical compositions. The typical mouthwash solutions Charles et al. (201) followed 108 volunteers for six months.
contain an antiseptic, such as chlorhexidine, cetylpyridinium One group rinsed twice daily with a commercial brand of
chloride, methyl salicylate, or providone-iodine. Other essential oil mouth rinse. A second group rinsed twice daily with
ingredients may include water, glycerin, flavoring, artificial chlorhexidine. A control group rinsed with 5% hydroalcohol. At
coloring, sweeteners, preservatives, emulsifiers, essential oils, and six months, dental exams demonstrated that essential oils mouth
other chemicals (173). Alcohol concentrations in some products rinse and chlorhexidine mouth rinse had comparable anti-plaque
may range from 5% to 17% and has been linked to oral mucosa and anti-gingivitis effectiveness. Safety concerns remain for
irritation and xerostomia (175, 176). Debate continues over the children, alcohol addicts, and those with ethanol metabolism
effectiveness of mouth rinses with different populations. deficiencies due to the alcohol content in some of these
Chlorhexidine is the most commonly used oral antiseptic agent mouth rinses (200).
among dentists and physicians in ICU and long-term care
facilities (177), but it has not been without its controversy. In the
ICU, ventilator-associated pneumonia (VAP) is the leading cause 4.2 Patient oral care programs
of death with a 50%–76% mortality rate (178). VAP is defined as
pneumonia developing more than 48 h after initiating mechanical 4.2.1 Oral assessment procedures
ventilation (179). Chan et al. (180) systematically reviewed 11 Patient care programs should, ideally, assess the health status of
studies totaling 3,242 mechanically-ventilated patients. Four the oral cavity periodically, especially in long-term care facilities.
studies (181–183) totaling 1,098 patients found that oral Assessment tools, such as the Minimal Data Set (MDS) or the
antibiotics did not significantly reduce the incidence of Resident Assessment Protocol (RAP), are administered at the
pneumonia, while seven studies (146, 173, 184–189) totaling time of admission, during an annual assessment, or if there has
2,144 patients reported that oral antiseptics, primarily been a significant change in the resident’s health status (202).
chlorhexidine, significantly reduced the incidence of VAP. These However, these devices may not examine the health of the oral
findings support other studies of chlorhexidine use (190–193). A tissues or other oral health-related issues presented by the patient
more recent systematic review of 17 studies by Keykha et al. or resident (203). The Geriatric Oral Health Assessment Index
(194) supports the use of chlorhexidine to reduce the incidence (GOHAI) helps physicians to identify psychosocial and
of VAP. However, their review also found chlorhexidine had only functional problems associated with oral health issues and to
a small effect on gram-negative resistant bacteria, which are the decide if a dental referral is needed. The Oral Health Impact
most common pathogens causing VAP. Pineda and associates Profile (OHIP), developed by Slade and Spencer (204), is an
(195) systematically reviewed four studies totaling 1,251 heart index of physical, social, and psychological descriptors, such as
surgery and ICU ventilator patients and concluded that the use trouble pronouncing words, worse taste, painful aching, self-
of the oral antiseptic agent chlorhexidine did not reduce the consciousness, embarrassment, unsatisfying life, etc. The 14-item
incidence of nosocomial pneumonia or the rate of mortality. shorter version is now in use world-wide (205). More recently,
Price and colleagues (196) report selective digestive and oral Campos and colleagues (206) questioned the validity of the
decontamination were superior to chlorhexidine in preventing OHIP as a multidimensional measurement. Their study reported
death in ICU patients, and, in fact, state that chlorhexidine was that the OHIP-14 works properly as a one-factor model for
associated with a higher rate of mortality in these populations. dentate patients only but not with non-dentate patients. Further,
Further, other studies have reported that chlorhexidine may they report that cultural context factors, such as orofacial
cause adverse oral mucosa effects including erosive oral lesions, appearance, or the impact of oral health on life, and age factors
bleeding, ulcerations, and white/yellow plaque (197, 198). could also influence responses, particularly among non-dentate
Additional evidence now suggests that the effectiveness of patients. As a measure of the patient’s perception of the impact
chlorhexidine may be pathogen-specific. Fourrier and colleagues of a given oral condition in their lives, Campos’ assessment of
(184) followed 228 non-edentulous patients with endotracheal the OHIP found it a valid measure. However, self-assessments by
intubation and mechanical ventilation for 28 days. The older patients or residents are not generally accurate and focus
experimental group received 0.2% chlorhexidine three times on remaining teeth. In addition, Kayser-Jones et al. (207) report
daily. Results showed no significant differences in the that more than two-thirds of residents have some level of
chlorhexidine group and the placebo group. Chlorhexidine did cognitive impairment and cannot report having caries or
not eradicate Pseudomonas aeruginosa, Acinetobacter, and oral discomfort.
Enterobacter bacterial species from the dental plaque. Some Kayser-Jones and colleagues (207) developed the Brief Oral
bacteria, such as Pseudomonas aeruginosa, form biofilms that Health Status Examination (BOHSE) to evaluate the oral health
protect them from immune invasion, antibiotics, and antiseptic of long-term care residents by the nursing staff. It is one of the
agents, such as chlorhexidine (195). The uncertainty remains and first screening tools developed to quickly examine ten oral health
the effectiveness of antiseptic mouthwashes may have to do more and function areas (lips, tongue, tissue of the cheek, the roof,

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and floor of the mouth, gingiva between the teeth or dentures, stays, and reduce the incidence of death (213–215). Thus, as a
saliva, condition of natural teeth and dentures, and oral preventative treatment, why isn’t oral cleaning a priority in acute
cleanliness). BOHSE uses a 3-point nominal scoring scale (0–2). care hospitals and long-term care facilities? Salamone and
A summed final score subjectively determines the health status of colleagues (211) state that oral health care is an essential duty of
the oral cavity. A modified version of the BOHSE is the Oral nursing care and is a part of a holistic approach including
Health Assessment Tool (OHAT), a tool designed to simplify the bathing and toileting, or “cares.” While it may be convenient
assessment categories and their descriptions. As a staff- when managing basic patient care duties, nursing should
administered screening device, it provides practical information consider separating oral hygiene from this “care package.” Oral
to the nursing staff and other care providers about oral hygiene hygiene should be reframed as a broader oral infection control
care for functionally dependent and cognitively impaired older procedure and receive the same focused care attention as an
adults and helps prevent development of biofilm-related diseases infected wound site (217).
in the oral cavity (201). The OHAT has eight categories and uses Yoon and Steel (217) argue that the use of a holistic approach
the 3-point nominal scoring scale (0-healthy, 1-oral changes, by caregivers is motivated by social factors and not by potential
2-unhealthy) used in the BOHSE. A summed score provides an health consequences related to poor oral hygiene. Lack of proper
overall level of oral health. Further, by adding categories for training and education of the nursing staff in oral health and
behavioral problems and oral pain, the results of the OHAT may care is a major concern, but implementation of newly learned
indicate the need for a referral for a dental assessment. Chalmers care skills is also a factor. Overall, nursing training programs
et al. (208) examined the reliability and validity of the OHAT vary in their emphasis on oral care training, and nursing
across 21 nursing care facilities and 455 residents. Amongst the textbooks typically include oral hygiene procedures for those
staff, intra-carer agreements were moderate for lips, saliva, oral patients unable to manage their own care (218). A survey of
cleanliness, and referral to a dentist (Kappa = 0.51–0.60), while recent nursing graduates found that they had a good basic
agreement on all other categories was substantial (Kappa—0.61– understanding of oral health, but a poorer knowledge and
0.81). Inter-carer Kappa statistics were similar to the intra-carer understanding of oral-systemic disease connection and how to
agreements. These results support the reliability and validity of screen or examine the oral cavity (219). Dahm et al. (220) report
the OHAT and its use in nursing care facilities as an oral that 1% to 3% of the nursing workforce is trained to provide oral
hygiene screening device. In a retrospective observational study, care to older adults with nursing assistants receiving the least
Maeda and Mori (209) examined 624 hospital-admitted patients training. Unavailable cleaning supplies, uncooperative patients,
over the age of 65 years. The purpose was to determine whether pressure of other duties, and fear of injury by the patient are
poor oral health could be a predictor of in-hospital mortality reasons given for poor nursing responses related to patient oral
within 60 days of the time of hospital admission. The patients hygiene care (211, 221, 222).
were divided into three groups using OHAT scores: (1) Group Elderly nursing home residents have extensive oral disease and
with OHAT scores of 0; (2) Group with scores of 1 & 2; and (3) poor oral hygiene (156). In a survey by Wårdh and associates (223),
Group with scores of >3. Patients with OHAT scores of >3 89% of nursing home staff considered oral health care for residents
showed a significantly higher mortality rate (18%) compared to important; 60% reported brushing teeth was a troublesome activity.
the other two groups. These patients were likely to be older, Eighty-percent (80%) reported uncooperative residents as a major
malnourished, cognitively impaired, and inactive. Primarily used issue. Similar findings were reported by Palmers and colleagues
in nursing care facilities, Simpelaere et al. (210) report the (224). Facility training programs for continuing education and
OHAT is a very good tool to assess hospital patients when new staff training in oral care have mixed reviews for
administered competently by the care staff, including nursing, effectiveness. Gammack and Pulisetty (225) report that a 30-min
nursing assistants, and speech pathologists. staff oral care training program with lecture, demonstrations, and
hands-on skill training did not result in significant changes in
4.2.2 Oral care as a medical treatment oral care activities and practices by the staff. Samson and
Oral care, while considered a common and routine hygiene colleagues (226) report that a well-organized program for nursing
task, is, in fact, a preventative medical treatment for potential home residents should emphasize motivating and oral-care
oral infection development. Its administration is recognized as a training of the staff, use of picture-based oral care cards,
basic nursing duty in hospitals and long-term care facilities in distribution of adequate oral care equipment, practical
most countries, but may be largely neglected (211, 212). It may implementation of new routines, and a means to assess outcomes
either be preventative or responsive. Preventive oral medical using the mucosal-plaque score index. To test this concept,
treatment is the routine or daily cleaning of the mouth to control Samson et al. assessed program effectiveness at three intervals:
bacteria growth and those conditions which may foster the start of the study, at 3 months and after 6 years. At the start of
development of disease and illness. Responsive oral medical the program, 36% of the residents had acceptable scores. Six
treatment is purposeful and aggressive oral cleaning for a years later, 70% showed acceptable scores. Ildarabadi and
debilitated person with a serious illness, and to prevent or reduce associates (227) implemented an 8-week oral care program in a
the risks of secondary illnesses (infections) from developing from nursing care facility. Improvement was not immediate, and
oral pathogens. Organized oral care programs reduce the required a minimum of four to eight weeks before improved oral
incidence of pneumonia, reduce febrile days, reduce hospital health status were noticeable.

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The Mouth Care Without a Battle is a program devised by prevent microaspiration of pathogen-laden saliva and mucous
Zimmerman and colleagues (228). It is a pragmatic program generated in the oral and pharyngeal cavities (236). Luk and
provided by nursing home staff emphasizing person-centered Chan (232) state that tube feeding should be a last resort and
support to improve the resident’s quality of life and support the should not be the rationale to prevent pneumonia. In a
well-being of the staff while providing oral hygiene care. The retrospective study of 63 patients receiving enteral feeding or
referenced paper provides a thorough and clear description of restricted oral foods, Maeda and Akagi (237) reported that a
the program supported by evidence, and goes well-beyond the formalized oral hygiene care program was effective. They used
scope of this review. In a subsequent paper, Zimmerman and two groups (control and an oral hygiene program group). The
colleagues (229) compared the Mouth Care Without a Battle incidence of pneumonia for the tube-fed or restricted oral
program with standard oral care in fourteen long-term care feeding group receiving formal oral care from the staff was
facilities. The incidence of BAP was reduced during the first year significantly less than in the control group (0.45 vs. 1.20). In
of the program, but was not significantly changed with the addition, oral care in the intervention group reduced febrile days,
special intervention program during the second year. reduced administration of antibiotics, and reduced the number of
Sustainability of first year improvement could not be maintained blood tests and radiographic studies taken.
despite staff booster training, and ongoing support. For effective
implementation and success of oral care programs in long-term 4.2.3 Professional oral care
care facilities, a program must be well-organized and Professional oral care provisions in health care facilities vary
documented protocols and procedures, must be administered by worldwide. Few hospitals in the United States provide inpatient
a full-time care program director, must have constant staff or outpatient dental services, with dentistry provided through
training, must have adequate equipment, must use valid and private dental practices, which is the universal model. An
reliable measure tools, must use visual tools both for the exception is the inpatient and outpatient dental services provided
staff and residents, must keep data and these data must be to military veterans by the U.S. Department of Veterans Affairs
shared with the staff, and it must have the full support of the hospitals. In many countries, dental services are funded through
facility’s administration. private pay or some form of private or government-supported
Jones and colleagues (230) surveyed intensive care unit (ICU) insurance. While long-term care facilities in the U.S. are federally
nurses regarding their priorities in providing oral care. Thirteen mandated to assess the oral health of their residents, few facilities
and a half percent (13.5%) rated oral care as a low priority, comply. The lack of dentist availability and costs prevent long-
85.5% reported using a toothbrush daily with patients, 50.5% term care facilities from providing onsite dental services (238).
routinely used chlorhexidine oral wash, and 23.5% of nurses had Use of dental hygienists has increased and has shown to be
not received training in oral care. However, in a later study by effective in preventing respiratory infections with nursing home
Sreenivasan et al. (231), a survey of 200 ICU nurses indicated all residents (239). Other facilities have utilized dental hygienists as
were aware of focal oral infection theory, 93% knew about staff coaches to implement and guide oral care programs, such as
potential complications from poor oral care, and 95% performed the Mouth Care without a Battle (240). More recently, several
oral care after every shift change. They reported the main barrier countries, such as the United Kingdom, Australia, and New
to oral care with ICU patients was mechanical obstruction Zealand, have created a new specialty, Oral Health Therapy
secondary to oral intubation and oxygen masks. (OHT). This specialty’s scope of practice includes oral health
Routine oral care neglect increases the possibility of oral-related assessment, examination, diagnosis and treatment planning,
complications with tube-fed or depressed consciousness patients. prevention, minimal intervention and health promotion as well
In the past, risks of potential aspiration pneumonia and as nonsurgical treatment of periodontal disease and dental caries.
decreased survival have been reasons for the use of tube feeding, In these countries, the OHT duties include some of the same
nasogastric (NG), or gastrostomy (232). The thinking by some duties of dental hygienists and dental therapists (241). OHTs
caregivers may be that these patients are not taking food and have become valuable resources long-term care facilities,
liquid orally, thus oral care is of lesser importance. Koichiro particularly with the frail elderly. However, many of the same
(233) describes how oral functions are suppressed in tube-fed or barriers exist as with dental hygienists including lack of
depressed consciousness patients and the oral environment is not opportunity, adequate education and training, poor pay, and
self-cleaned. As a result, mucosal resting saliva mixes with the having adequate equipment (242).
oral residue to form a sticky paste-like biofilm that adheres to Weekly professional, mechanical cleaning vs. daily antiseptic
the oral cavity and teeth surfaces. Reduced salivary washing and disinfecting decreases or eliminates oropharyngeal bacteria in the
mucosa replacement do not remove this biofilm from the oral dependent elderly (243). Adachi and colleagues (244) followed
surfaces and form a coating on the tongue. Dysbiosis of the oral 141 elderly nursing home residents for two years. Those
flora allows respiratory pathogens to colonize these thick biofilms receiving professional oral care weekly had significantly reduced
and is a viable source for pathogenic aspirate. Blumenstein and fevers and fatal BAP when compared to a control group of
colleagues (234) report that poor oral hygiene was found in tube- residents receiving routine daily care. Similarly, Ishikawa et al.
fed patients with an aspiration incidence of 89%. Juan et al. (243) followed three cohorts receiving staggered routines of
(235) report a pneumonia rate of 31% in a group of continuous professional care for five months. Results showed that bacteria
tube-fed stroke patients. Alternative feeding avenues do not counts were significantly lower in all three groups following

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professional care for 5- and 3-month periods. At 3 months, group 3 specific and stipulate the type of infections causing the
began receiving professional care and with significant reductions in pneumonia, such as Staphylococcus pneumonia, Staphylococcus
Streptococci and Candida. Febrile days increased for group one aureus pneumonia, or Klebsiella pneumonia. Adopting the use of
(not significant) and group two (significant) but decreased in this microbe-based terminology clinically helps differentiate it
group three. The effects of the cold and flu season during the from other terms used for aspiration pneumonia and provides
study influenced the latter findings. Pneumonia developed in 8 clarity of meaning for care providers much the same as “viral
residents in group one and no cases in group two or three pneumonia” differentiates itself from bacteria-based pneumonias.
during the experimental period. In a study by Sjögren and As discussed, for pneumonia to develop, the environment of
colleagues (245), oral care significantly reduced mortality when the oral cavity must be dysbiotic with impaired airway protection
provided by dental personnel compared with the care and compromised lower respiratory immunity. The Three Pillars
administered by the nursing staff. Further, the incidence of of Bacterial Aspiration Pneumonia model brings focus to these
mortality did not significantly change with nursing staff three primary factors. This model identifies serious illness (Pillar
administered oral care. Finally, in a seminal study, Yoneyama I), poor oral health (Pillar II), and laryngotracheal impairment
et al. (246) randomly assigned 417 nursing home residents to (Pillar III) as the primary components that must be present
one of two groups: oral care group and no-oral care group. The together for bacterial pneumonia to develop (18–20). If this
no-care group received routine oral care, while the care group model is inclusive of all factors needed for BAP development, it
received daily assistance from caregivers and nurses, and dentists may differ from other models because it places the health status
or dental hygienists visited weekly to provide professional care. of the oral cavity and it’s aspirate as key factors, and holding
This organized oral care program significantly reduced the equal or higher importance than the biomechanical inefficiency
occurrence of pneumonia, febrile days, and death in this of the larynx resulting in aspiration. Many papers have presented
population. The inclusion of professional oral care successfully excellent definitions of aspiration pneumonia, and the “Sekizawa
reduces the incidence of pneumonia by as much as 40% among Definition” provided by the Japanese Respiratory Society in 2009
the elderly in the care group (213). While professional dental (15) is exemplary for its guidance in pneumonia diagnoses. But,
services are not widely available in many countries, in those like many descriptors, it focuses on the identification and
countries where it is provided the incidence of pneumonia and diagnosis of pneumonia and not on its source, the oral cavity. To
death in residents in long-term care facilities is reduced. include the importance and complexity of an unhealthy oral
cavity environment to pneumonia development helps to better
frame the complexity of pneumonia, particularly in clinical
5 Discussion assessments and interventions. Bacteria aspiration pneumonia
may be defined as the result of biomechanical and sensory
Pathogenic flora residing in the oral cavity cause local and inefficiency or impairment of the protective laryngeal valving
systemic diseases including periodontal disease and bacterial mechanism allowing virulent pathogens originating in the oral
aspiration pneumonia. This narrative review examines this cavity to enter an immunocompromised lower respiratory system
complex ecosystem and how it changes with aging and impaired and infecting the lung parenchyma.
health status. These changes can potentially trigger a cascade of To augment the human immune system efforts to control
microbiological events that result in local and other systemic pathobiome development, oral hygiene care works to control and
diseases. This review does not include aspiration of gastric reduce biofilm accumulations of pathogen colonies on oral
contents, or aspiration pneumonitis. The intended focus is to surfaces. Toothbrushing regularly is the number one method in
examine the complexity of the oral cavity environment, its reducing biofilms from the surfaces of teeth, the primary sites of
microbiome, its pathological changes that lead to development of bacterial attachment. Controversy over the use of chlorhexidine
BAP, and the effectiveness of oral care intervention in the has not been definitively resolved. While it appears in many
prevention of BAP. studies to effectively reduce bacterial load and prevent BAP
The term, “bacterial aspiration pneumonia,” is used in this development, questions remain over its effective dose, potential
review as it has appeared in many prior publications side effects, population-specific outcomes, and its impact on
(221, 247–250) in place of the commonly used term, “aspiration motality. The validity of chlorhexidine use in specific populations
pneumonia.” This particular terminology specifically emphasizes remains unclear and further double-blind studies are needed (251).
that bacteria is the required component when aspiration from Oral hygiene care seems simple enough. Pressing and
the oropharynx results in pneumonia. Further, this term scrubbing a bristle brush against the surfaces of the teeth.
distinguishes bacteria aspiration pneumonia from other terms However, when caring for others, this seemingly simple task may
often used to imply pulmonary infection, such as “aspiration often be overlooked, neglected, or too challenging for caregivers.
pneumonitis,” “post-obstructive pneumonia,” “community- Nursing assistants or aides are given the task with little medical
acquired pneumonia,” “ventilator-associated pneumonia,” or knowledge of the oral cavity or how to properly provide oral
“hospital-acquired pneumonia.” Many of these terms rely on cleaning. Even for the educated caregiver, patient, or nursing
descriptors of population or environment locations, implied home resident, oral cleaning processes may be difficult and time-
equipment-associated causes, or other conditions rather than the consuming. Often, proper equipment, products, and assistance
underlying bacterial pathogen cause. Some designators are more are not available. And, providing care to disruptive patients or

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residents becomes even more challenging for the staff. Successful Author contributions
programs are presented and referenced in this paper and have
shown ongoing staff education, leadership, and teamwork JA: Conceptualization, Investigation, Writing – original draft,
provide the best results for the patients and residents. Oral Writing – review & editing.
hygiene prevents diseases and facilitates a better quality of life for
patients. This fact should elevate its importance in all care
facilities-hospitals and long-term care facilities-toward disease
prevention. Oral care or oral hygiene tasks should be recognized Funding
and elevated to the status of oral infection control.
While this review can only be considered cursory, much more The author declares that no financial support was received for
is known about the importance of oral health through a rich and the research, authorship, and/or publication of this article.
vast repository of studies, data and findings. The evidence that
oral pathogens cause systemic diseases is not new. Wadsworth
(172) told us so over a hundred years ago. And, evidence Acknowledgments
supporting oral cleaning as the best intervention to help prevent
these diseases is not new and very plentiful. The questions then The author wishes to thank Michelle Skelly, Matthew Ward,
are (1) why is oral health and oral cleaning not a primary focus Sherri Coker, and Edward Bice for their support and critical
in healthcare and disease prevention, and (2) why is preventative feedback in manuscript preparation.
and restorative oral health care not considered on an equal basis
as other medical care for payment support, such as insurance
and governments-supported health care plans?
Conflict of interest
JA is co-owner and Education and Research Director of SA
6 Conclusions Swallowing Services, PLLC.

Oral hygiene care, if utilized as a medical treatment, prevents

systemic disease, particularly bacterial aspiration pneumonia.
While acknowledged as a patient-care procedure, oral cleaning is Publisher’s note
overlooked or neglected in hospitals and nursing care facilities.
Poor staff training, lack of supplies, and unsupportive All claims expressed in this article are solely those of the
administrators are the primary obstacles in providing this authors and do not necessarily represent those of their affiliated
preventative care to hospital patients and nursing home organizations, or those of the publisher, the editors and the
residents. Concerted and well-organized preventative oral care reviewers. Any product that may be evaluated in this article, or
program reduce the incidence of pneumonia and death and claim that may be made by its manufacturer, is not guaranteed
improve patient quality of life. or endorsed by the publisher.

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