Introduction

Dysphagia is common after stroke from the acute phase through to the chronic phase and is significantly associated with the development of pneumonia from aspiration [1]. Post-stroke pneumonia also increases mortality, morbidity, and medical costs [2•, 3]. Dysphagia and malnutrition are the main risk factors of pneumonia following stroke [4], the former of which increases the chance of aspirating not only foods when eating, but also saliva secretions. Dysphagia rehabilitation and diet modification can lower the risk of aspiration pneumonia. For instance, the bypass of food passage with gastric tubing prevents the aspiration of chewed food or liquid, although regurgitation remains a threat. Moreover, even if oral food intake is halted, the aspiration of saliva cannot be avoided completely since it is constitutively secreted. The oral health of stroke patients is often deteriorated as well as overlooked. Poor oral hygiene increases the likelihood of aspirating oral pathogenic bacteria with saliva and ensuing aspiration pneumonia. Since saliva aspiration cannot be completely prevented in dysphagic stroke patients, it becomes essential to improve the quality of aspirated saliva by maintaining good oral and pharyngeal health. Thus, during stroke recovery, oral health is as important as dysphagia rehabilitation to prevent local and systemic disorders.

The Importance of Oral Health in Stroke Recovery

The Role of Saliva

A total 1–1.5 L of saliva is secreted and swallowed daily in normal individuals. Saliva has several important roles in promoting oral health: enzymes and immunoglobulins in the saliva control the colonization of microorganisms in the oral cavity and reduce biofilm build-up on the tooth surface, while mucin protects the mucosal membrane from ulceration via its lubricating properties. Saliva is also a buffer that neutralizes acid produced by bacteria or gastric acid before it reaches the oral cavity by gastro-esophageal reflux or regurgitation. Oral digestive enzymes, including amylase and lipase, decompose starch and lipids to help digestion. Before swallowing, saliva lubricates the food to assist in optimized bolus formation on the tongue surface during mastication.

Oral health conditions often deteriorate under hospital or nursing home care in stroke patients, which provides a favorable condition for the formation of dental plaque biofilm. Poor oral hygiene may produce dental caries and periodontal disease and increase the risk of systemic complications [1, 5]. As stroke patients often present with compromised oral hygiene [5, 6], aerobic gram-negative bacilli are frequently observed in acute stroke patients and are associated with mortality [7]. The oral pathogenic bacteria subsequently flow into the pharynx mixed with saliva. Dysphagic individuals have difficulty dealing with normal amounts of salivary secretion, resulting in overflow aspiration.

Dental Biofilm Formation in the Oral Cavity

Oral pathogenic bacteria are considered to be the cause of aspiration pneumonia [8], infective endocarditis, and the other systemic diseases [9]. The composition of microorganisms in the oral cavity includes hundreds of species of bacteria [10], most of which are normal flora that control the balance of bacterial species and suppress the colonization of foreign microorganisms in the oral cavity for host protection. To survive in such environments containing saliva and antimicrobial peptides [11], oral microorganisms attach to host surfaces and begin biofilm formation. Bacterial dental plaque is a dynamic environment composed of an extracellular matrix containing a complex community of many bacterial species [12]. The bacteria create colonies and interact with each other within the glycocalyx, an extracellular capsular polysaccharide matrix. Approximately 108 oral bacteria exist in 1 mg of dental plaque. Oral bacteria forms biofilm on both hard and soft tissues in the oral cavity, including the tooth surface, tongue surface, gingival sulcus, pharynx, and saliva [13], and therefore pathogenic periodontal bacteria can be detected even in edentulous individuals [14].

The composition of bacterial flora in the mouth is diverse and depends on location [10]. Oral bacteria are often sub-categorized according to their need for oxygen. As oxygen concentration is relatively high on the surface of soft tissues, aerobic bacteria and fungi readily colonize in these areas. In contrast, anaerobic bacteria tend to predominate in the periodontal pocket or gingival sulcus, where oxygen concentration is less than 1 %. The species of colonizing bacteria change depending on the stage of oral biofilm formation [12]. In the early period, colonizers include many types of oral streptococci and other natural microbiota, which are not known as respiratory pathogens [10]. In the later stages of colonization, the biofilm microenvironment becomes anaerobic and suitable for more pathogenic colonizers, such as Fusobacterium nucleatum, Tannerella forsythia, Treponema denticola, and Porphyromonas gingivalis, to populate the biofilm and increase the risk of systemic infections [15, 16]. These earlier and later colonizers exhibit interspecies adhesive interactions to enhance biofilm formation.

Periodontal Disease and the Incidence of Stroke

Frequently associated with atherosclerosis and stroke [17•, 18, 19], periodontal disease is a chronic infectious condition characterized by a gradual loss of periodontal connective tissue and alveolar bone support. Dental plaque accumulating in the periodontal pocket is a cause of gingival tissue inflammation. The gram-negative bacteria in the plaque and their secreted endotoxins invade blood vessels from inflamed tissues to trigger inflammatory responses in blood vessel walls and produce inflammatory cytokines that further promote atherosclerosis. Several meta-analyses have presented strong evidence associating periodontal disease and tooth loss with the occurrence of stroke [17•, 18, 19]. Thus, although poor oral hygiene is often witnessed in stroke patients due to insufficient oral care in admitted hospitals [5, 6], oral health may have already been compromised before the onset of stroke.

Oral Health Care in Stroke Recovery

Pneumonia is a severe complication of stroke that increases mortality [20]. Dysphagia elevates the risk of pneumonia at all stages of stroke recovery, from the acute phase in the intensive care unit (ICU) through to the rehabilitation period [2•]. In the ICU, stroke patients are often mechanically ventilated by endotracheal intubation, which may cause respiratory infection via the intubation tube [21, 22]. On the other hand, the incidence of pneumonia is also high in community-dwelling patients with cerebrovascular disease [23]. Pneumonia in nursing home residents and the dependent elderly is termed HCAP. Many admitted patients with HCAP have dysphagia, and thus are considered to have aspiration pneumonia [23, 24]. There are numerous studies describing the benefits of oral care on the prevention of ventilator-associated pneumonia (VAP) and other forms of pneumonia in hospital and nursing home patients.

Oral Health Care During Acute Phase Stroke Recovery

The incidence of pneumonia is 6–20 times higher in patients who receive mechanical ventilation in the ICU [25]. VAP prolongs the length of stay in the ICU and increases mortality and medical costs [26, 27]. Bacterial colonization of the oral cavity is considered to be a reservoir for respiratory pathogens [8]. During intubation, oral bacteria count may increase from secretion accumulation, suppressed swallowing reflex, or low consciousness level as critically ill patients in the ICU are often unconscious or sedated. Patients receiving mechanical endotracheal ventilation have a risk of aspirating contaminated secretions pooled in the oral cavity or pharynx, such that deep sedation has been discouraged for ventilated patients since it increases the risk of aspiration.

The microorganisms contained in the biofilm forming on the endotracheal tube during intubation have been associated with the onset of VAP [28]. Biofilm develops on both the inside and outside of the tube. Although the endotracheal tube cuff is designed to block the leakage of saliva from the oropharynx, it does not protect the lower airway completely since the inflated cuff has folds. As a result, some secretions reach the subglottal area. The distal end of the endotracheal tube was found to have a greater diversity of microorganisms [28]. Thus, continuous subglottic secretion drainage above the cuff during endotracheal intubation can reduce VAP risk by eliminating pooled secretions that leak down to the trachea [29]. Oropharyngeal dysphagia often remains after extubation of the endotracheal tube [30]. Accordingly, the maintenance of oral health is also important at this time, and patients should avoid aspirating secretions or contaminated rinsing water since subglottal suction is impossible once the tube is removed.

Hospitalized stroke patients frequently exhibit an inability to brush their teeth due to hemiplegia or cognitive problems. Assistance by caregivers is therefore needed to maintain oral hygiene and prevent pneumonia. There are many studies describing the effectiveness of oral care on pneumonia avoidance, particularly in hospitalized and critically ill patients [5, 31, 32, 33•]. Established oral care protocols can enhance effectiveness and decrease the risk of aspiration pneumonia [32]; and mechanical dental plaque removal with a toothbrush along with the use of sponge swabs, a tongue scraper, and/or chemical decontamination with chlorhexidine (CHX) have been broadly introduced in many regimens [5, 31, 34]. Shi et al. conducted a meta-analysis on the effect of CHX on VAP prevention in critically ill patients [33•]. In over 17 randomized control trials, mechanical oral care with CHX provided a significant reduction in VAP over regimes without CHX (OR 0.60, 95 % CI 0.47–0.77).

Oral Health Care After Hospital Discharge

Pneumonia remains a common complication after discharge from the hospital after stroke. Pneumonia is classified as hospital-acquired pneumonia (HAP), community-acquired pneumonia (CAP), and healthcare-associated pneumonia (HCAP). A relatively new category, HCAP includes any patient who was hospitalized in an acute care hospital for two or more days within 90 days of the infection; resided in a nursing home or long-term care facility; received recent intravenous antibiotic therapy, chemotherapy, or wound care in the past 30 days of the current infection; or undergoes hemodialysis [35]. Carratala reported that patients with HCAP were older and had greater comorbidity [23], such as cerebrovascular disease. Aspiration pneumonia was also significantly more frequently encountered in patients with HCAP than in those with CAP [23, 24]. Dysphagia is relatively common in such individuals, who are therefore more prone to aspiration. A recent study has also demonstrated oral health to be associated with quality of life among nursing home residents and stroke patients at home [36•, 37]. Although reports on oral care in community-dwelling patients are relatively few compared with those on hospitalized patients, several have found significant reductions in the risk of pneumonia by formal oral care regimens in nursing home residents [38], while others have shown that professional oral care by dental hygienists decreases the risk of pneumonia and influenza [39]. The procedures for nursing home residents included mechanical cleaning using a tooth brush, sponge swab, and/or tongue scraper. Dentures were cleaned with a denture brush. Less is known on chemical cleaning using CHX, which is more popular and supported in hospitalized patients, especially those with endotracheal ventilation.

Oral Care Procedures

Dysphagia increases the risk of aspiration pneumonia, but this can be reduced by regular oral care. The amount of displaced contaminants rises in the oral cavity by the mechanical removal of dental plaque [40], at which time prompt elimination has an important role in preventing their aspiration. However, rinsing of residual oral contaminants carries the risk of aspiration as rinse water can easily reach the pharynx due to its rheological properties, the patient’s diminished consciousness, and gravity. Ikeda et al. reported that removing contaminants with mouth wipes after mechanical brushing significantly reduced the amount of oral bacteria without rinsing, indicating that this method may be a suitable alternative because of no additional fluid [40].

The Hygiene of Dentures

Many stroke patients are elderly individuals who wear dentures. Denture hygiene deteriorates easily and proper fitting is lost when the oral condition is neglected during prolonged hospital stays. The surface of dentures is rough and hydrophobic, both of which are amenable to the formation of biofilm. Denture plaque and candidiasis colonies gradually accumulate if the denture or its contact teeth are not adequately cleaned. Poor hygiene of the denture surface and denture plaque are prominent risk factors for denture stomatitis (i.e., local infection), and recent literature has indicated that they are predisposing elements for pneumonia (i.e., systemic infection) as well [41, 42•].

Continuous denture wearing during sleep is also associated with diminished oral hygiene and leads to biofilm formation on the denture surface. There are numerous respiratory pathogens on the denture surface [41, 43]. The swallowing reflex becomes dull when unconscious, resulting in the silent aspiration of contaminated saliva secretions. Iinuma et al. reported that the risk of pneumonia doubled when the dentures were worn during sleep [42•]. Taken together with the above findings, proper cleaning of dentures and their removal while sleeping is imperative in dysphagic stroke patients with high aspiration risk to decrease the chance of pneumonia.

For cleaning, dentures should be removed from the mouth and scrubbed with a denture brush. As this does not prevent subsequent biofilm formation on the denture surface, chemical cleaning by soaking in a commercial disinfectant solution is also important after brushing [44].

Conclusions

The oral health of stroke patients deteriorates easily, which increases the risk of local and systemic infections. To prevent aspiration pneumonia, exercises that enhance swallowing ability as well as oral health care are essential. It is necessary to maintain oral health care from the acute phase through to the chronic phase of stroke recovery. In the acute phase, VAP is the most serious respiratory complication and should be prevented by oral care to decrease the mortality of stroke. Chemical cleaning with CHX along with mechanical oral care is effective in avoiding this outcome. The maintenance of good oral health in stroke patients remains important in rehabilitation and nursing homes. In the chronic phase, oral care performed by stroke patients themselves is often inadequate due to hemiplegia and may require assistance. After the mechanical removal of oral contaminants, mouth wipes may be a suitable alternative to rinsing and suctioning. Removal and proper cleaning of dentures will also aid in the prevention of aspiration pneumonia and improve prognosis in stroke patients.