New horizons in understanding oral health and swallowing function within the context of frailty

Abstract

Frailty is a complex and multidimensional condition wherein declines in physiologic reserve and function place individuals in a state of heightened vulnerability and decreased resiliency. There has been growing interest in both research and clinical settings to understand how to best define, assess and characterise frailty in older adults. To this end, various models and clinical assessment tools have been used to define and measure frailty. While differences exist among these models and tools, a common unifying theme is a focus on physical function and activity. Notably absent across many available conceptual models and clinical tools are items directly related to oral and swallowing function. This is an important oversight as widespread changes to both oral and swallowing function are evident in older adults. Indeed, emerging evidence suggests many of the functional domains affected in frail older adults, such as nutrition and sarcopenia, have cyclical relationships with impairments in oral (oral hypofunction) and swallowing function (dysphagia) as well. The increasing appreciation for the interrelationships among oral hypofunction, dysphagia and frailty provides an opportunity for refinement of frailty assessment and characterisation in older adults to incorporate metrics specific to oral and swallowing function.

Key Points

• Impairments in oral health and swallowing function are increasingly recognised as being associated with frailty.

• Oral hypofunction and dysphagia are notably absent from many conceptualisations of frailty despite observed relationships.

• Care and management of frail older adults may be enhanced by including oral health and swallowing metrics in frailty assessments.

Introduction

Since the time of its historical origin, the concept of frailty has evolved into numerous theories and models, which have precluded a well-agreed-upon definition and characterisation [1]. Despite lack of consensus, a common theme among existing frailty models is the focus on limb function and ability to complete activities of daily living [2–5]. This is likely due to sarcopenia, or age-related decline in muscle mass and strength [6], being considered a main component of frailty [7]. While sarcopenia has mostly been studied in terms of its effects on limb function, bulbar-innervated muscles of the head and neck important for oral and swallowing function are also affected [8, 9].

Oral and swallowing functions are vital to overall health as they facilitate oral intake and hydration necessary for physical function and survival [10, 11]. Recent investigations note oral health factors, such as number of teeth and mastication, are associated with frailty [12]. Similarly, studies examining the relationship between swallowing dysfunction (dysphagia) and physical frailty in older adults have found: (1) dysphagia is associated with early signs of frailty [13]; (2) self-reported dysphagia is an independent predictor of frailty [14]; (3) dysphagia may be more prevalent in hospitalised patients who are pre-frail and frail [15]; and (4) dysphagia that co-occurs with frailty can be more severe and associated with higher 1-year mortality rates compared to those with frailty without dysphagia [16].

Emerging evidence details the associations among oral hypofunction, dysphagia and frailty; however, oral and swallowing function are often overlooked in the conceptualisation of frailty. This results in missed opportunities to assess, identify and manage these impairments in frail, older adults. This paper seeks to expand upon and formalise concepts previously overviewed [12, 16–21] which, collectively, underscore the importance and relevance of oral health and swallowing function to frailty.

Methods

This Horizons review is the result of a multidisciplinary working group composed of speech-language pathologists, a physiotherapist, a dentist and physicians with experience and expertise in ageing, oral health and/or swallowing function who sought to describe the role of oral hypofunction and dysphagia in the development of frailty. Our working group met via videoconference monthly from November 2020 through April 2021 to discuss oral health and swallowing-related factors as they relate to ageing and frailty. Through literature searches and discussions, we constructed and progressively revised a frailty framework that uniquely incorporates the concepts of oral hypofunction and dysphagia (Figure 1). In this paper, we present the four components of frailty and highlight areas of interaction with oral and swallowing function derived from our working group: (1) primary drivers, (2) pathologic manifestations, (3) exacerbating factors and (4) contextual factors. Primary drivers facilitate a transition into a frail state. Pathologic manifestations are the specific physiologic impairments that stem from the primary drivers. Exacerbating factors tend to worsen pathologic manifestations by creating additional stress on already compromised physiologic systems. Finally, homeostenosis and contextual factors are discussed as underlying mediators that can influence individual trajectories across the other components.

Figure 1.

An overview of components related to the clinical conceptualization of frailty. Facetsof oral hypofunction and dysphagia (represented by light green boxes), which have historically gone unrecognized in the conceptualization of frailty, are also considered in the broader context of frailty development. Components of frailty that have direct associations to oral hypofunction and dysphagia are represented with dark green boxes.

Primary drivers

Ageing

Ageing produces deterioration at the cellular, tissue and organ levels which results in decreased function, reduced adaptability to stress and, eventually, death [22]. While ageing represents a global, whole-body decline in maintaining homeodynamics, frailty is more centred upon failure to sustain homeodynamics relating to energy metabolism and neuromuscular changes [23]. Frailty risk increases with age, with speculation that all individuals would succumb to frailty if they lived long enough [24, 25]. Thus, the underlying biological processes (e.g. apoptosis) occurring in ageing are likely accelerated in frailty [23]. Among the primary drivers of frailty, ageing is perhaps the most important, as it accounts for many of the physical and physiological changes underlying interrelationships among oral hypofunction, dysphagia and frailty. These specific age-related changes are discussed in greater detail below.

Multimorbidity

Multimorbidity, or the coexistence of two or more diseases/conditions within an individual, carries an approximately 2-fold increased risk for frailty [25, 26]. Impairments in oral health and swallowing function are potential contributing factors and/or consequences of multimorbidity. For example, multimorbidity is commonly associated with polypharmacy that can result in hyposalivation. This can increase susceptibility to dental decay and pneumonia via disruption of the oral microflora [27, 28] and negatively impact eating due to altered taste and olfaction [29]. Additionally, safe and efficient swallowing depends on cross-system interactions. Specifically, there are interactions across the physical (muscular/mechanical), cognitive (neurological), oral, gastrointestinal and pulmonary systems during swallowing [30]. These interactions allow performance in one system to impact performance—either as harmful or beneficial—in or across other systems.

Malnutrition

Malnutrition has been suggested as a single-pathway mechanism in frailty [24, 25]. Frailty assessments, therefore, will often include an item related to nutrition, such as unintentional weight loss [31]. Further, ‘nutritional frailty’ has been proposed as a frailty subtype and represents a targeted mechanism for at-risk individuals or those in the early (and reversible) stage [25].

A recent meta-analysis revealed that the pooled prevalence of malnutrition in community-dwelling, older adults reached almost 25% [32], and these prevalence rates can be higher when dysphagia [33] and comprised oral health status [34, 35] are present. Oral hypofunction and dysphagia are upstream from malnutrition and can be attributed to factors such as difficulty chewing and hyposalivation [36, 37]. These impairments can impede oral intake, and may result in increased meal duration [38] and decreased energy intake [39, 40], which can create an energy imbalance. Modified diets are often used to accommodate reduced oral function and dysphagia; however, these diets often contain insufficient nutritional content. Further, individuals may be dissatisfied with items offered under modified diets [39, 41] or be reluctant to consume items non-integral to their culture [42]. Given findings that both the quantity (nutrient intake) and quality (types of nutrients) of nutrition are relevant to frailty [43], these disruptions to oral intake have broader implications for frailty.

Pathologic manifestations

Physical

A key pathophysiologic component of frailty is loss of overall physical function stemming from sarcopenic effects on limb and bulbar musculature [6, 44]. Several studies have highlighted the impact of sarcopenia of the tongue—a primary muscle involved in oral health and swallowing—on the ability to swallow effectively [45–47] and these effects may have greater implications for frail older adults.

Muscle homeostasis is typically maintained by a balance between the formation of new muscle cells, hypertrophy and protein loss coordinated by the neurological, endocrine and immune systems [2]. This balance is further influenced by nutritional factors and physical activity level [2]. Frailty can adversely affect muscle homeostasis, resulting in accelerated development of sarcopenia [2]. There are many causal interactive mechanisms in the development of sarcopenia and frailty, including oxidative stress, dysregulation of inflammatory cytokines and hormones, malnutrition, physical inactivity and muscle apoptosis [6, 48].

Dysphagia

The relationship between physical frailty and dysphagia is at least partially mediated by sarcopenic effects on swallowing musculature [49]. With frailty, extensive changes in muscle function may impair swallowing musculature strength and coordinating movements resulting in disordered mastication, inefficient bolus transport and increased airway invasion risk [16, 20, 21]. Further, older adults may have impaired airway defence mechanisms (e.g. impaired mucociliary clearance) placing them at increased risk for pulmonary complications, including pneumonia, if airway invasion occurs [50]. Additionally, the cerebral cortex modulates the brain stem swallowing network through descending inputs that allow for changes based on bolus properties (volume, viscosity, taste, etc.) [51]; however, neural activation in key brain regions active during swallowing has also been shown to be reduced in older adults [52], which increases the risk of dysphagia.

Oral hypofunction

Developing research indicates that dental caries, tooth loss, periodontitis and oral pain are associated with oral motor hypofunction and frailty. Oral pain and disfigurement negatively impact productivity [53] and can exacerbate social withdrawal, isolation and low self-esteem [54]—factors that have been found to increase the risk of developing frailty in older adults [55]. Periodontitis, a source of chronic inflammation, is associated with several systemic diseases including diabetes, Alzheimer’s disease and cardiovascular diseases [56], which can worsen frailty. Changes to taste and smell may reduce hunger, particularly in older adults, and in conjunction with tooth loss and sarcopenia of the swallowing musculature, increases the risk of developing malnutrition [57]. It is unclear whether managing tooth loss by wearing removable dental prostheses (i.e. dentures) may positively influence these outcomes. A recent study found that partial denture wearers had normal nutrition status and increased dietary intake compared to those without dentures and complete dentures, respectively [58]. However, other investigations note an increased risk of developing malnutrition and frailty secondary to wearing dental prostheses [34, 37, 59]. A systematic review found that wearing dentures positively impacts eating-related quality of life; however, there was no clear effect on diet, suggesting other aspects of oral health and/or oral motor hypofunction may be important [60].

Cognitive

Late-life cognitive decline is recognised as an important component of frailty and contributes to adverse outcomes, including morbidity and early mortality [61, 62]. Similar to the nutritional frailty subtype, ‘cognitive frailty’ has also been proposed as a subtype involving physical frailty and cognitive dysfunction [62]. Despite the increasing attention on cognitive frailty, this functional domain (along with swallowing and oral health) is often not included in frailty assessment tools [62]. This oversight is notable given the interrelationships between swallowing function, oral health and nutrition with cognitive function in both healthy and patient populations that have been established [63–65].

Although previously thought of as a ‘reflex’ response mediated by the brainstem, neuroimaging studies have revealed a far more diffuse, complex distribution of neural regions associated with swallowing, including shared areas recognised for their involvement in cognitive processes [66]. Cognitive awareness of food/liquid material is required to initiate self-feeding behaviours even before a bolus is introduced into the oral cavity [67, 68]. Cerebral areas controlling higher-level cognitive processes, such as language and attention, have also been found to be active during swallowing [69]. A decline in cognitive function, therefore, can impact swallowing behaviours. There has also been increasing interest in the relationship between cognitive function and oral health, particularly in older adults as the incidence of oral diseases increases with age [70]. A systematic review of longitudinal studies by Wu et al. [70] revealed equivocal findings surrounding oral health measures (dentition condition, denture use) and cognitive impairment. A more recent meta-analysis performed on 14 longitudinal studies [71] revealed an approximately 1.5-fold increase in the risk of cognitive impairment for individuals with tooth loss. Causality, however, continues to be debated.

Exacerbating factors

Acute illness

Instances of acute illness, particularly in those requiring emergency department and/or inpatient care, can trigger frailty and exacerbate an existing frail state in at-risk older adults [72, 73]. New or worsening impairments in oral health and swallowing function are common outcomes in the acute care setting and, as such, may amplify the effects of frailty in vulnerable older patients experiencing an acute illness. Importantly, poor oral health is an independent, in-hospital predictor of mortality [74]. Poor oral health is prevalent upon admission to acute care settings [75] and oral health tends to deteriorate during acute care hospitalisations, particularly in mechanically ventilated intensive care unit (ICU) patients [76]. Previous studies note that the teeth and other oral surfaces of patients in the ICU become ‘breeding grounds’ for respiratory pathogen colonisation, which along with factors such as impaired oral clearance, impaired airway clearance and impaired immune response may lead to the development of pneumonia [50, 76–80].

Dysphagia affects up to 47% of hospitalised frail older adults [81] and is characterised by airway invasion and oropharyngeal residue [16]. A recent investigation found the presence of dysphagia and frailty in a cohort of hospitalised patients was consistently associated with longer length of hospital stay (LOS), increased healthcare costs, non-routine discharges and medical complications [20]. Similar to poor oral health, dysphagia is a predictor of mortality, with adult patients with dysphagia 1.7 times more likely to die in the hospital as compared to patients without dysphagia [82]. Among survivors, those with dysphagia have a mean LOS approximately 2.8 days longer and are more likely to be discharged to a post-acute facility compared to patients without dysphagia [82]. These outcomes highlight that reduced oral health and dysphagia in the acute care setting carries an increased physical toll that frail older adults with decreased functional capacity and resiliency may tolerate poorly.

Healthcare interventions

The relationship between acute illness and frailty is intensified with more severe illnesses that require increased levels of medical and/or surgical intervention. For instance, medications such as antipsychotics, diuretics, local anaesthesia and muscle relaxants may have anticholinergic, antimuscarinic, antihistaminic or neuromuscular blocking properties which can lead to dry mouth (hyposalivation) and/or impaired action of muscles important for deglutition [83]. Mechanical ventilation is commonly used in older adults with critical illness and frailty [84] and serves as an independent risk factor for developing adverse health outcomes such as post-ICU frailty [85]. Post-extubation dysphagia occurs in up to 62% of patients requiring mechanical ventilation and has been found to persist after discharge. Further, post-extubation dysphagia is associated with poor health outcomes, such as feeding tube placement, pneumonia and in-hospital mortality [85]. Diet modifications are another healthcare intervention often initiated to maintain nutrition and hydration in patients with difficulty eating and swallowing. However, achieving adequate nutrition and hydration with these diets is difficult, impacts overall physical function and contributes to the vicious cycle of frailty (see Malnutrition section).

Contextual factors

The interrelationships among oral and swallowing dysfunction and frailty are complex and multidimensional. Thus, we cannot limit our understanding to the physical implications, but must also consider contextual factors. These underlying sociodemographic determinants of health such as race, neighbourhood deprivation and access to healthcare and resources likely influence the extent to which one experiences the individual and synergistic effects of frailty, oral hypofunction and dysphagia.

Research in this area has found: (1) non-Hispanic Black and Mexican American older adults have a higher prevalence of untreated cavities than non-Hispanic White older adults; (2) the rate of untreated cavities is three times higher in older adults with less versus higher education; and (3) older adults with lower income, less education and who smoke are more than three times likely to have complete tooth loss in ageing as compared to their counterparts [53]. There is a paucity of literature surrounding contextual factors and dysphagia risk; however, a recent longitudinal investigation found area deprivation was associated with increased odds of dysphagia [86]. Generally, contextual factors such as lower income, less education, poor lifestyle choices (smoking, being sedentary, etc.) and neighbourhood deprivation are more prevalent among individuals classified as frail [63–65]. The importance of these factors in the broader context of frailty was previously underscored by Whitson and colleagues who sought to distinguish frailty stemming from isolated physiologic impairments (‘phrailty’) from frailty due to interactions between functional limitations, psychosocial and environmental factors (functional ‘f-frailty’) [87].

These contextual factors should not only be considered in weighing the risk for frailty, oral hypofunction and dysphagia but should also be considered when managing these impairments. For example, if a frail, older adult with poor oral health requires extensive dental management, do they have transportation to their appointments? Do they have adequate dental insurance coverage? If a frail, older adult with dysphagia is recommended to consume certain food textures, does their local grocery store offer a variety of nutritious options at a cost within their food budget? These examples highlight the additional complexities surrounding these interrelationships that should be contemplated in clinical decision-making.

Homeostenosis

Central to the concept of frailty and the aforementioned factors is homeostenosis or the narrowing of functional reserves needed for homeostasis [3, 88]. Functional reserves are excess physiologic capacities that are used to maintain homeostasis when an individual is faced with stressors [3, 88–90]. Adequate reserve indicates an individual has the physiological resiliency to withstand homeostatic challenges [91]. Progressive reserve loss in the sensory, metabolic, cardiac, gastrointestinal, etc. systems during ageing and with frailty can result in impaired function (i.e. pathologic manifestations) noted in the oral, swallowing, physical, nutritive and cognitive domains [2, 91–95]. As reserve is lost in one system, the body will compensate by relying upon other functional reserves to maintain function [88]. In turn, functional reserves available to tolerate new challenges are outweighed by functional reserves already in use (Figure 2) [88]. At this point, individuals are considered ‘frail’ due to widespread reductions in their physiologic capacities and little to no ability to withstand physiologic stressors [3, 88, 91].

Figure 2.

A conceptual representation of homeostenosis based on previous work by Taffett [88]. In the early stages of the lifespan, there is adequate functional reserve throughout the body’s structures and physiologic systems to tolerate physiologic stressors. In this healthy state, individuals are in the ‘safe’ zone where the amount of functional reserve outweighs the amount of functional reserve in use. With ageing, there are progressive declines in functional reserve (homeostenosis) and physiologic capacity. This decline in functional capacity necessitates that more functional reserves are employed to maintain baseline function which places individuals in a ‘danger’ zone where they have very little functional reserve available to tolerate physiologic stressors.

While the term ‘homeostenosis’ is typically not used in the context of oral health and swallowing, reduced reserves in these systems can be reasonably inferred from literature that indicates age-related alterations across the oral health and swallowing continuum [96–98]. Still, these changes do not necessarily result in oral hypofunction or dysphagia, likely because most physiologic systems contain 4 to 10 times more reserve than what is needed for baseline function [99]. Therefore, some older adults with minimal reserve loss will maintain their oral and swallowing functions, while frail older adults who tend to suffer greater declines in functional reserve [2, 100] may have increased difficulty sustaining these functions. More research is needed to determine if functional thresholds exist to differentiate between expected, age-related declines and pathological reductions in oral and swallowing function.

Moving towards the new horizon

It is our view that the emerging evidence illustrating interrelationships among oral hypofunction, dysphagia, ageing and frailty provides an opportunity to reconceptualise what it means for one to age successfully. Namely, along with conventional approaches (e.g. not smoking, exercising, etc.) [101], maintaining oral health to prevent oral diseases/disability and preserving swallowing function to meet daily nutrition and hydration needs are also inherent to ageing well. Thus, greater attention to oral health and swallowing function in older adults, particularly those at risk for frailty, is needed. Our hope moving forward is: (1) integrated assessment approaches in the primary care setting; (2) interprofessional education and training with a specific focus on oral and swallowing function; and (3) awareness initiatives geared towards increased understanding and identification of impairments in oral and swallowing function in older adults at risk for frailty.

Integrated healthcare approaches, wherein an interprofessional team addresses the needs of patients requiring complex care, have been shown to improve continuity and quality of care, reduce healthcare costs, and spare negative health outcomes [102–105]. Primary care settings serving patients at risk of frailty could consider establishing or expanding upon currently established multidisciplinary teams to include oral health and swallowing specialists to improve patient care. When this multidisciplinary team approach is infeasible due to staffing, costs, etc., screenings may identify at-risk patients. There are several validated screeners for oral health (e.g. Oral Health Assessment Tool [106], Kayser-Kones Brief Oral Health Status Examination [107]) and swallowing function (e.g. 3-ounce Water Swallow Test [108], Eating Assessment Tool-10 [109]) that could be used as part of an integrated approach.

To facilitate this interdisciplinary model of care, the current curricula of medical, dental, nursing and rehabilitation (i.e. SLP) professionals need to ensure a focus on interprofessional learning that encourages a strong integration between oral health care providers, swallowing specialists and primary care providers. Oral healthcare-related training and education detailing the role of swallowing function in maintaining nutritional homeostasis are necessary, important and relevant for healthcare providers outside the fields of Dentistry and Speech-Language Pathology. Given that the functional changes that accompany ageing and frailty are multifaceted and do not typically occur in isolation [24, 110, 111], specialties involved in the care of older adults cannot work in a silo. Didactic training needs to be expanded so healthcare practitioners are made aware of how functions relevant to their specialty may influence other functions and outcomes. However, this integrated approach will depend upon a crucial step—raising awareness.

Raising awareness of the importance of oral health and swallowing function to ageing and frailty both at the general public and medical provider levels is crucial. Many initiatives, such as the United Nations Decade of Aging and Aging in Place, have emerged over time emphasising activities (maintaining social activities and physical activity) and dimensions of care (improving the person-environment, integrated healthcare approaches) that help promote health and longevity in older adults [112, 113]. Several awareness programmes have been established on the local level that focus on increasing awareness of the importance of oral health in older adults and underserved populations [114–116]. However, there is a need for national programmes to be established that promote awareness of oral health maintenance and the value of good oral health to reduce frailty, and how both are interrelated and can affect successful ageing. This is particularly important in older adults experiencing pre-frailty or frailty as they likely have complex health needs and as such, maintaining oral health may be overlooked or viewed as less of a priority. In addition, a concerted effort needs to be made to bring awareness and establish initiatives that communicate the importance of preserving healthy swallowing function during the lifespan to ensure adequate nutrition and hydration are maintained in old age. Swallowing changes in older adults may not be entirely obvious given that swallowing function cannot be visualised and may be as subtle as taking longer to eat a meal. Thus, public health initiatives that are geared towards increasing understanding and awareness of swallowing difficulties that may be encountered in ageing and how to address these concerns with a primary healthcare provider may help prevent these issues from escalating and creating additional burdens for older adults with and without frailty.

Conclusion

The goal of this paper is to raise awareness of the bidirectional relationship between oral health, swallowing function and frailty to improve identification and management of these impairments in at-risk and frail older adults through employment of an interprofessional approach. The interrelatedness of the outlined factors may offer clinicians the opportunity to reap benefits from a single targeted intervention that provides benefits across multiple impairments. We hope the information presented here will be used to expand upon available frailty models and assessment tools to consider including oral health and swallowing function metrics. Future work should examine themes identified in specific patient populations to better understand the unique contribution of different disease processes to the overall development of oral hypofunction, dysphagia and, ultimately, frailty. Such work will allow potentially modifiable targets to be identified and managed earlier which may help circumvent the deleterious effects of frailty.

Declaration of Conflicts of Interest

Dr Nicole Rogus-Pulia is a VA employee. The content and views expressed in this article are those of the authors and do not necessarily reflect the position or official policies of the US Government or the US Department of Veterans Affairs. The remaining authors have no relevant disclosures.

Declaration of Sources of Funding

This work was supported by the National Institute on Aging (8K00AG076123-03 to Dr Robison and 1K76AG068590 to Dr Rogus-Pulia) and the National Institute of Dental Craniofacial Research (DE028271A to Dr Yeh). This work was also partially supported by the William S. Middleton Veteran Affairs Hospital, Madison, WI (Dr Rogus-Pulia, GRECC Manuscript 002-2023). The funding organisations were not involved in the study conceptualisation, review or approval of the manuscript or the decision to submit the manuscript for publication.