Geroscience: Aging and Oral Health Research

Abstract

Research in aging has significantly advanced; scientists are now able to identify interventions that slow the biologic aging processes (i.e., the “hallmarks of aging”), thus delaying the onset and progression of multiple diseases, including oral conditions. Presentations given during the 3-part session “Geroscience: Aging and Oral Health Research,” held during the 2023 American Association for Dental, Oral, and Craniofacial Research meeting, are summarized in this publication. Speakers’ topics spanned the translational research spectrum. Session 1 provided an overview of the geroscience and health span (disease-free and functional health throughout life) concepts. The common molecular mechanisms between oral cancer and aging were discussed, and research was presented that showed periodontal microflora as a potential factor in Alzheimer’s disease progression. Session 2 focused on behavioral and social science aspects of aging and their oral health significance. The keynote provided evidence that loneliness and isolation can have major health effects. These social conditions, along with poor oral health, tooth loss, and cognitive decline, could potentially affect healthy eating ability and systemic health in older adults. Research could help elucidate the directions and pathways connecting these seemingly disparate conditions. Session 3 focused on the delivery of oral care in different settings and the many barriers to access care faced by older adults. Research is needed to identify and implement effective technology and strategies to improve access to dental care, including new delivery and financing mechanisms, workforce models, interprofessional provider education and practice, and use of big data from medical–dental integration of electronic health records. Research to improve the “oral health span,” reduce oral health disparities, and increase health equity must be tackled at all levels from biologic pathways to social determinants of health and health policies.

Introduction

Background of the American Association for Dental, Oral, and Craniofacial Research Meeting within a Meeting

As part of the American Association for Dental, Oral, and Craniofacial Research (AADOCR) science-first initiative to bring new opportunities for membership, professional development, and program growth, the AADOCR initiated a Meeting within a Meeting (MwM) featuring cutting-edge presentations on broader themes in dental, oral, and craniofacial (DOC) science. The first MwM in March 2022 featured Contemporary Artificial Intelligence Applications in Dental Research, oriented toward both dental researchers and clinicians to build a shared terminology for contemporary research and to welcome researchers new to DOC science.

This report summarizes the second MwM held during the annual session of the AADOCR and the Canadian Association for Dental Research at the Oregon Convention Center in Portland, Oregon, March 15 to 17, 2023. The topic, Geroscience: Aging and Oral Health Research, is based on a trans–National Institutes of Health (NIH) research initiative (NIH, National Institute on Aging n.d.-a, n.d.-b). It was also partly inspired by the United Nations declaration of 2021 to 2030 as the “UN Decade of Healthy Ageing” (United Nations General Assembly 2020). Over the 3 d, speakers referred to evidence on the prolongation of a healthy life span through research that covers the translational research spectrum: biologic pathways; animal and human studies; behavioral, social, and policy aspects of aging and their effects on oral health and disease; and gaps in our knowledge. Research and training to improve care delivery among older adults are urgently needed. AADOCR is grateful for the unrestricted educational grant received from Haleon to support expenses associated with this meeting.

MwM Objectives

1. Provide a broad overview of the concept of geroscience, how it is connected to the biological mechanisms of aging and age-related disease, and how these associations impact health span, quality of life, and oral diseases

2. Provide a holistic overview of social and behavioral aspects of aging, particularly related to loneliness, social isolation, tooth loss, nutrition, and cognitive decline

3. Propose research needed to improve the delivery of oral health care for aging populations

4. Encourage researchers who study aging to include oral health conditions and diseases

5. Inspire DOC researchers to study older adult populations.

The proceedings of this MwM have been organized within this report to reflect the translational synergy across the 3 daily educational sessions. Days 1 and 2 each featured a keynote speaker followed by 2 shorter talks by DOC researchers. Day 3 featured 4 short talks from AADOCR members. A brief time period was available for questions, comments, and discussion with the audience.

Theme 1: Biological Aspects of Aging

Keynote: Geroscience: Biological Aging and Oral Health

Geroscience is the field of research that seeks to define mechanisms linking biological aging with age-related functional decline and disease (Kennedy et al. 2014). Biological age is the greatest risk factor for nearly every major cause of death and disability in developed countries (Lombard et al. 2016; Kaeberlein 2019). The risk of dying from cancer, heart disease, or COVID-19, for example, goes up approximately 30-fold between ages 45 and 85. The risk of developing Alzheimer’s disease increases approximately 300-fold over that same time frame (Fig. 1). Although not as well appreciated, age is also the leading risk factor for many diseases of the oral cavity, including periodontal disease and oral cancers (An et al. 2018).

Figure 1.

Aging is the greatest risk factor for most diseases. Forty years of biological aging has a much greater impact on risk of death from cancer (all types), heart disease, COVID-19, or Alzheimer’s disease compared to other common risk factors. Risk values for alcohol, smoking, obesity, hypertension, and APOE (e4/e4) are an approximation from surveying published studies. Risk resulting from 40 y of aging between ages 45 and 85 is shown and was obtained as the ratio of the risk of death for each condition at age 85 divided by the risk of death at age 45 as listed in the US Centers for Disease Control Wonder Database for 2020. In 2020, heart disease, cancer, and COVID-19 were the 3 most common causes of death in the United States.

The mechanisms underlying biological aging have become better understood over the past 20 y, allowing for conceptual formalization of key “Hallmarks of Aging” (López-Otín et al. 2013). These hallmarks are interconnected (Fig. 2) and appear to be regulated by a highly conserved network of interacting genes, proteins, and metabolites. In principle, any or all of the hallmarks of aging represent therapeutically useful targets through which it may be possible to attenuate biological aging. For example, “senolytics” represent a class of drugs that aim to selectively kill senescent cells (one of the hallmarks of aging), a strategy shown to increase life span in rodents and the subject of numerous current clinical trials (Wissler Gerdes et al. 2021). Such interventions have the potential to be far more effective than current disease-specific approaches because they delay the onset and progression of multiple age-related diseases simultaneously and thereby increase both life expectancy and health span, which is defined as the period of life spent free from chronic disease and disability (Fig. 3).

Figure 2.

Interconnected hallmarks of aging. The hallmarks of aging represent several interacting processes that are shared features of biological aging across the animal kingdom. These hallmarks represent potentially useful targets for therapeutic intervention to increase health span and prevent age-related disease. The hallmarks of aging should not be considered a comprehensive explanation of biological aging but instead serves as a conceptual framework for our current understanding of the aging process.

Figure 3.

Slowing aging is more effective than curing disease. The impact of curing disease on life expectancy for a typical 50-y-old woman in the United States can be estimated from data collected by the Centers for Disease Control and Prevention. Curing either of the 2 largest killers (cancer and heart disease) increases life expectancy by 3 to 5 y and curing them both by less than 10 y. In contrast, delaying aging to an extent comparable to the effects of rapamycin or caloric restriction on life span in rodents has a proportionally much larger effect on life expectancy, with the added benefit that most of those years are spent in good health, free from chronic disease and disability. Figure generated from data presented in Lombard et al. (2016). Coloring illustrates hypothetical impact on health expectancy in each case, where green represents absence of comorbidity and red represents severe comorbidity.

The drug rapamycin is a specific and potent inhibitor of the mechanistic target of rapamycin (mTOR) that has been shown to increase life span and delay or reverse age-associated functional decline and pathology in numerous tissues and organs in laboratory animals, including mice (Johnson et al. 2013). Of relevance to oral health, transient treatment with rapamycin in aged mice is sufficient to reverse multiple features of periodontal disease associated with normative aging, including regrowth of bone around the teeth, a reduction in gingival inflammation, and remodeling of the oral microbiome toward a more youthful composition (An et al. 2020). The RAPID (Rapamycin in Adults with Periodontal Disease) clinical trial (unpublished data) will seek to determine whether rapamycin can similarly reverse periodontal disease in people. Rapamycin and additional therapeutics designed to modulate the biology of aging present a particularly promising strategy to improve oral health in aging populations.

Oral Cancer and Aging

Oral cancer increases with age, peaking between ages 60 and 70. Aging and cancer are highly interrelated as they share numerous underlying mechanisms. Several common molecular mechanisms are involved in aging and oral cancer, including DNA damage, cellular senescence, and immunosenescence (Berben et al. 2021).

Accumulation of cellular damage is a critical driver in aging and cancer. Lifelong exposure to endogenous (e.g., free radicals) and exogenous (e.g., alcohol, tobacco, foods) stress factors can induce an increase of oxidative stress, leading to genomic instability/DNA damage. When DNA repair mechanisms fail, apoptotic or senescence programs are activated to eliminate mutations that can lead to cell transformation and tumor initiation. Cellular senescence is a key driver of the aging process. Activated by DNA damage or telomere shortening, senescent cells enter a state of irreversible growth arrest, yet remain metabolically active. A cellular hallmark of cellular senescence is the senescence-associated secretory phenotype (SASP), where long-term expression of multiple SASP factors contributes to “inflammaging,” defined as the age-related increase in levels of proinflammatory mediators in blood and tissues that can modify the tumor environment. Changes in both myeloid and lymphoid immune cells occur during the aging process. The number of both naive T and B cells is decreased, but the number of memory T and B cells is increased. In addition, antigen recognition and presentation capabilities are reduced. Finally, the number and function of myeloid-derived suppressor cells and macrophages are increased that greatly contribute toward a highly immunosuppressive tumor microenvironment (Lian et al. 2020).

A recent study used publicly available data sets from The Cancer Genome Atlas (TCGA) to relate aging-related genes and the prognosis, inflammation, and tumor immunity of head and neck squamous cell carcinoma (HNSCC; Yang et al. 2020). A risk model was developed for a subset of aging-related genes associated with immunosuppression, suggesting a prognostic genetic signature, which could be used for individualized immunotherapy. Thus, it is critical for aging to be considered a biological modifier in oral cancer disease progression. Use of age-appropriate mouse models and human subjects that reflect biological and/or chronological aspects of aging must be considered to deepen our understanding of aging influences on oral cancer to discover better treatments.

Alzheimer’s and Periodontal Disease

While slower processing speed, difficulties sustaining attention, multitasking, and other cognitive changes are common problems in later life, cognitive impairments (e.g., memory loss, language impairment, and deficits in executive function) are typical manifestations of Alzheimer’s disease, a disease characterized pathologically by accumulation of beta-amyloid plaques, tau-tangles, and inflammatory activation of glial cells in the brain. Over the past several decades, treatment of Alzheimer’s disease has focused on strategies to prevent the accumulation of beta-amyloid deposits in the brain through a variety of “antiamyloid” approaches. As most of these approaches have been met with some to limited success to support the role of amyloid accumulation as a primary driver of Alzheimer’s disease, attention has also been devoted to targeting potential upstream causation events prior to some of the irreversible pathological changes in the brain. Studies on the translocation of microbiota and their microbial products from biofilms in periodontal disease, in particular the keystone pathogen Porphyromonas gingivalis (Ilievski et al. 2018) and its key family of gingipain proteases, support one possible upstream causation event in the development of Alzheimer’s disease (Dominy et al. 2019). From these studies, a 48-wk multicenter US Food and Drug Administration (FDA) phase 2/3 randomized controlled clinical trial demonstrated that 1 small-molecule inhibitor of gingipain significantly reduced the rate of loss of cognitive function by approximately 50% in participants (n = 643) with either P. gingivalis detected in saliva (38%) or with an elevated antibody response to P. gingivalis (50%). Due to safety concerns regarding transient liver toxicity, a second series of small-molecule inhibitors with an improved safety profile from FDA phase 1 studies is planned for phase 2 FDA clinical trials. This study demonstrates that specific targeting of a key periodontal pathogen supports the role of translocation of periodontal microflora as 1 potential upstream causation event in the progression of Alzheimer’s disease for at-risk populations (Detke et al. 2023). In addition, future personalized dentistry/medicine approaches may include lifestyle modification and microbial testing to identify patients at risk of developing Alzheimer’s disease before overt clinical systems arise. These targeted antimicrobial approaches may be combined with lifestyle modification, novel anti-inflammatory therapies (Kantarci et al. 2018), new antiamyloid and antitau tangle therapies, and conventional periodontal treatment approaches to remove pathogenic biofilms.

Day 1 Discussion

Age is a leading risk factor for many diseases of the oral cavity, including periodontal disease and oral cancers, as well as common systemic diseases, like Alzheimer’s disease. Common mechanistic pathways that intersect these diseases in aging involve DNA damage, cellular senescence, immunosenescence, and inflammaging. Upstream events that may trigger these mechanisms, such as an altered inflammatory state in susceptible individuals, include the onset of oral dysbiosis. Targeting these specific upstream events, selecting common inflammatory pathways, or using personalized therapies are current and future approaches that hold promise to address the hallmarks of aging.

Theme 2: Behavioral and Social Science Aspects of Aging and Oral Health Significance

The US population 65 y of age and older is growing rapidly and is on course to outnumber the younger population by 2034 (National Institutes of Health [NIH], National Institute of Dental and Craniofacial Research [NIDCR] 2021b). Along with this significant increase, research on associations of health and oral health with aging has grown. Poor physical and mental health and higher mortality risk are associated with, to name a few, a person’s number of remaining teeth, their oral function, nutritional status, and a variety of self-assessed behaviors (e.g., tooth brushing, diet, annual dental visits), as well as their social health and nutrient intake (Paganini-Hill et al. 2011; Rouxel et al. 2016). Assessing the association between oral health and the social aspects of aging has also grown in the past 2 decades, and health care professionals have begun to recognize and address the role of loneliness in decreased overall health (Freedman and Nicolle 2020). Vivek Murthy, the 19th and 21st US Surgeon General, released a 2023 Surgeon General’s Advisory calling attention to the epidemic of loneliness and isolation and the “healing effects of social connection and community.” The advisory describes how this epidemic increases the risk of disease and premature death and provides a guide for solutions. In surveys, the prevalence of adults reporting loneliness exceeds the number with diabetes, obesity, or smokers and thus must be considered by health care professionals as an important predictor of health and longevity (US Surgeon General 2023).

Keynote: Loneliness and Isolation in Older Adults: A Medical and Public Health Perspective

The irony of loneliness is we all feel it at the same time—together. —Rupi Kaur (2017)

The evidence demonstrating that loneliness and isolation have profound health effects has been growing over several decades. This evidence, together with current demographic transitions leading to increasing numbers of older adults, is forcing health professionals and researchers to rethink the ways that social connections affect all aspects of our lives, particularly as we age. Indeed, social isolation and loneliness are medical issues (Holt-Lunstad and Perissinotto 2023).

Loneliness, the subjective feeling of being isolated, and social isolation, the quantifiable number of connections with others, both affect our health in different and profound ways, from tooth loss to cognitive impairment and all-cause mortality (National Academies of Sciences, Engineering, and Medicine 2020). Prevalence rates of loneliness and social isolation in older adults have been estimated at 43% and 25%, respectively. It is because of these prevalence rates and the associated health effects that social isolation and loneliness must be viewed as modifiable risks with public health implications. Research should investigate the ensuing distress for the individual and cost implications, with determinations made to create interventions to reduce the extent of these conditions.

While this evidence on the health effects is established, some argue that addressing social concerns should not fall under the purview of health care professionals, while others believe that social disconnection should be addressed in health care encounters. However, there is limited evidence on how to do this. As an answer to these concerns, Holt-Lunstad and Perissinotto (2023) published the EAR framework to guide clinicians. The framework, like other frameworks already used in medicine, proposes to Educate (E) people on the importance of prioritizing social connection to offset the risks of staying lonely or isolated. The second step is Assessment (A) and involves using standardized measures of social isolation to uncover what someone is experiencing and to what degree, as well as track how someone does over time. The final step is to Respond (R). The response entails reassessing, customizing interventions to the individual, and, in a sense, socially prescribing.

The challenge is that the evidence for specific interventions is still evolving. Some interventions are promising and show that connecting people based on trust and shared interests can have dramatic effects (Kotwal et al. 2021). Ultimately, as the National Academies of Sciences, Engineering, and Medicine (2020) concluded in the Report on Loneliness and Isolation, we must continue to translate research into practice, strengthen education and training, improve awareness, and strengthen ties between the health care system and community-based networks. The Surgeon General’s advisory echoes the National Academy of Sciences report and goes further by discussing that many sectors have a role in addressing the loneliness epidemic across the life span. The resulting policy implications are many and, ultimately, involve incentivizing health care systems and providers to assess loneliness and isolation, as well as to include social programs as part of health care benefits. At a broader level, this also requires us to reconsider the social fabric that enshrouds us and ensure that it does not unravel, which would leave us unhealthy and at risk for premature death. In many ways, addressing social isolation and loneliness offers the clinician-researcher a unique opportunity to meld the clinical and research worlds and meet patient needs at both the bench and the bedside.

Oral Health and Nutrition in Aging

Nutrition risk factors in aging, including physiological, psychological, neurological, functional, and socioeconomic factors, negatively affecting a person’s appetite, dietary intake, and, ultimately, nutritional status and oral health. Oral conditions, including oral pain, tooth loss, and hyposalivation, cause difficulty biting, chewing, and swallowing and disturb the eating experience while increasing the risk for malnutrition (Zelig et al. 2019; Honeywell et al. 2022; Hussein et al. 2022; Moynihan and Varghese 2022; Dent et al. 2023). Hyposalivation, xerostomia, and altered taste due to medications and comorbid conditions also affect eating ability.

Difficulty eating negatively affects diet and nutrient intake, as well as eating-related quality of life (ERQOL). Social isolation, dietary restrictions due to chronic diseases, cognitive and physical disabilities, and economic challenges compound eating problems. These negative impacts on lifestyle, diet, and nutritional status increase the risk for malnutrition (Zelig et al. 2019; Honeywell et al. 2022; Hussein et al. 2022; Moynihan and Varghese 2022). Hussein et al. (2022) found that older adults with chewing problems are at almost twice the risk of malnutrition than those without.

Comorbid conditions exacerbate the risk of malnutrition (Honeywell et al. 2022). After controlling for comorbid conditions, Honeywell et al. (2022) found that the odds of malnutrition were 46% lower for those with functional dentition. Every additional unit increase in number of teeth or the number of posterior occluding teeth pairs was associated with 3% or 13% lower odds of being at risk for or having malnutrition, respectively (Honeywell et al. 2022). Older adults with edentulism and those lacking functional dentition are at a significantly greater risk for malnutrition, poor diet quality, and low ERQOL than those with at least functional dentition (Honeywell et al. 2022; Moynihan and Varghese 2022).

Older adults with tooth loss develop adaptive and maladaptive eating behaviors. Adaptive behaviors include changing food consistencies (e.g., peeling, mincing, mashing, cooking, pureeing) for eating healthy foods (Zelig et al. 2019). Maladaptive behaviors include avoiding nutrient-rich foods like fruits, vegetables, nuts/seeds, meats, and grains (Zelig et al. 2019). While prior research has demonstrated the negative impact of tooth loss on nutrition status and diet quality of this population, there is a dearth of research on approaches to reduce oral dysfunction and improve ERQOL and nutrition status in older adults with tooth loss, with and without dentures.

Not all older adults seek dentures to replace missing teeth; interprofessional efforts involving dentists, registered dietitians, and behaviorists are needed to design and test strategies to reduce oral dysfunction for those with tooth loss and those receiving dentures to improve ERQOL, diet behaviors, diet quality, nutrient intake, and nutrition status.

Tooth Loss and Cognitive Decline

In 2021, over 6.2 million older adults in the United States were living with Alzheimer’s disease and related dementia (ADRD), and the cost of ADRD was $355 billion (Alzheimer’s Association 2021). As cognitive decline is one of the main predictors of ADRD, identifying risk factors and pathways underlying cognitive decline will inform interventions to prevent and delay ADRD. Identifying individuals at risk for diminished cognitive function is essential for planning strategies to prevent the onset and progression of dementia. Recently, increasing attention has been devoted to understanding the association between tooth loss and diminished cognitive function.

A recent systematic review reported that adults with greater tooth loss had a 1.48 times higher risk of developing cognitive impairment and 1.28 times higher risk of being diagnosed with dementia, even after controlling for other factors (Qi et al. 2021). Meta-analysis results show that each additional missing tooth was associated with a 1.4% increased risk of cognitive impairment and 1.1% increased risk of dementia diagnosis. Preisser and colleagues (2022) found that cognitive status, a dichotomous variable derived from a summary of several cognitive tests in the Health and Retirement Study, was one of the predictors of 12-y incident edentulism in a validated 7-variable model. In their study, Kang et al. (2020) demonstrated a reciprocal relationship between oral health and cognitive function, whereby poor oral health contributed to impaired cognitive function, and likewise, poor cognitive function was associated with compromised oral health.

Diabetes and poor oral health are common among older adults. A US study using a nationally representative cohort of 9,948 older adults reported that the effects of the co-occurrence of diabetes and edentulism or one of these conditions alone on cognitive decline varied across different age groups: for adults aged 65 to 74, co-occurring diabetes and edentulism was associated with worse cognitive function and an accelerated rate of cognitive decline compared with those with neither condition (Wu et al. 2023). Also, they found that edentulism is associated with diminished cognitive function for the group of 65- to 74-y-olds, in addition to faster cognitive decline in both study age groups (65–74 y and 75–84 y). Yet, diabetes alone contributed to a faster cognitive decline only in the group 65 to 74 y.

In summary, epidemiological studies have shown an association between tooth loss and cognitive decline, in which many used self-reported oral health measures. While there are many theories, there is a lack of empirical evidence on the causal relationship between tooth loss and cognitive decline. Future studies are needed using clinical measures of oral health in longitudinal studies. Similarly, there is a large body of epidemiological evidence from cross-sectional and some longitudinal studies that demonstrates an association of periodontal diseases with cognitive decline. Further studies are needed to further understand the possible underlying mechanisms for a causal relationship between these 2 diseases.

Day 2 Discussion

Older adults are at risk of tooth loss and adverse oral conditions, cognitive decline, impaired societal functioning, poor diet, and malnutrition, and these factors are interconnected. Translational studies and implementation research are needed to design and test interprofessional interventions for individuals with tooth loss and those receiving dentures to reduce oral dysfunction and social isolation to improve dietary behaviors, food quality, nutrient intake, nutrition status, and ERQOL, as well as systemic and behavioral health. There may be multiple aging and societal pathways that connect these factors with different sequences of events. Interprofessional training and collaboration of future health professionals in dentistry, nutrition, medicine, mental health, and other professions are needed to implement solutions to reduce the cycle of impacts of oral dysfunction on nutrition, loneliness, social isolation, and systemic health in older adults.

Theme 3: Research Needed to Improve Delivery of Care of Older Adults

Delivery of Oral Health Care in Institutional and Home-Based Settings: Research Needed

Research on the delivery of oral health care in institutional and home-based settings exists in the areas of clinical care, workforce, education, policy, and funding. However, even with this body of knowledge, its translation and implementation into strategies for improved access to dental care in older populations have been limited. It has been proposed that, with improved education or funding, oral health care and long-term care providers, patients, and caregivers would value oral health care and thus provide and/or demand it. Although education and funding are critical, research initiatives must also be translated into improved clinical interventions and outcomes; new care models, as well as effective workforce models, must be implemented. In addition, barriers to care, including financial limitations (lack of insurance and low income), lack of transportation, lack of oral health care providers, and medical, cognitive, functional, and behavioral challenges, must also be addressed.

In a value-based care oral health US model, dental providers are paid to care for a population, with incentives for demonstrating value through preventing dental disease and keeping patients healthy (DentaQuest 2019). The incorporation of value-based care models into the practice of dentistry and increased governmental funding for oral health care are likely to have the most impacts on geriatric oral health care and the delivery of care in institutional and home-based settings in the coming decade. To ensure appropriate translation and implementation of value-based measures, researchers need to provide recommendations, as well as expertise, using proper study designs and research measures. Furthermore, researchers should be involved in the education of and collaboration with clinical providers and insurance companies. As value-based incentive payments will not solve the insufficiency of preventive care funding, reliable mechanisms to adequately reimburse preventive care are needed.

Currently, there are no national standards of care for mobile dental care and, in some states, minimal accountability for mobile dental providers. Research initiatives are needed to educate directors of long-term care facilities to develop, adopt, and enforce standards of oral health care for their residents, as well as to hold mobile dental providers and on-site care staff accountable in providing needed preventive care. This proposed research into interdisciplinary, interprofessional models of care and ownership of care will require multisource collaborative funding and the implementation of cost-effective workforce models.

An Approach from a Dental Provider Network: Research Needed

Clinical provider networks can contribute important insights about the effectiveness of clinical practice, workforce, and policy strategies relating to the oral health of older adults. As a critical dental access and safety net provider, Apple Tree Dental in Minnesota provides a unique perspective on how to integrate research into a clinical provider network to improve dental access for underserved long-term care residents. Apple Tree Dental was founded in 1985 to overcome barriers to oral health of older adults residing in long-term care facilities such as ageism, lack of staff training, experience, and priorities, through a Community Collaborative Practice model of care delivery. Leadership understood the value of robust recordkeeping for internal quality improvement and generating evidence for clinical and policy innovation; they built a custom electronic dental record to track dental status, recommendations, and treatments, including a custom dental diagnosis classification system.

By participating in Apple Tree’s comprehensive and continuous place-based model of care delivery, 44% of older adults in long-term care settings achieved oral health stability, defined as no new treatment needs at an oral evaluation following completion of initial treatment recommendations (Smith and Shay 2005). In a workforce case study, about 80% of procedures rendered within a long-term care facility were within the scope of an advanced dental therapist (Helgeson et al. 2018). Comparison of dental care between new outpatient and long-term care senior patients showed that costs decreased over time in both groups and that dental utilization patterns of these 2 groups also shifted over time to increased preventive care and decreased restorative care (Smith et al. 2020).

As a clinical provider organization, Apple Tree recognizes the synergy of clinical experience and robust data with research expertise to create much-needed evidence within a learning health systems (LHS) framework. Convening learning communities to engage in LHS learning cycles creates evidence to drive clinical practice innovations and policy change that can improve oral health outcomes for older adults and other vulnerable populations. Apple Tree Dental has advocated for strong partnerships between community clinical provider organizations and traditional research infrastructure and expertise. Effective cross-sector collaborations require use of a bidirectional translational science framework, as well as inclusive funding mechanisms to support these nontraditional research collaborations.

Future Directions for Oral Health Research and Aging

D’Souza reminded us that the Oral Health in America Report (NIH, NIDCR 2021b) has a specific section devoted to older adults that summarizes the demographics of this age group and the challenges they face with regard to access to care and the prevalence of oral and systemic conditions. With an aging population, more older adults need dental care related to repair and replacement of dental restorations. Many older adults have one or more chronic conditions for which they take medications. Many of these health conditions and medications cause xerostomia (dry mouth), which diminishes oral function. Chronic inflammatory conditions that are common to older Americans, such as cardiovascular disease and diabetes, are also associated with inflammatory dental diseases, such as periodontitis. They also need oral hygiene care and other preventive services. Many older adults are in long-term care settings or are homebound. Oral health disparities (e.g., periodontitis, edentulism) exist by gender, race/ethnicity, and poverty status. Smokers have a much higher prevalence of periodontitis than nonsmokers. Complicating matters, many adults lose their private dental insurance when they retire, leaving them with little to no coverage during a stage of life when their need for oral health care may be greater than ever.

NIH-funded research has advanced our understanding of basic mechanisms and clinical connections of oral–systemic comorbidities observed in elderly populations. Preclinical research has highlighted the mechanistic underpinnings of inflammaging in chronic pathologies, such as arthritis following the onset of periodontitis, the utility of gerostatic drugs in addressing periodontal bone inflammation, and the effect of hormones on women’s oral microbiome in periodontal disease, burning mouth syndrome, and/or other health conditions. Clinical studies in older adult cohorts have demonstrated an association between oral health problems and frailty/disability, including reduced muscle strength and physical performance, poor diet quality, higher risk of dementia and Alzheimer’s disease, and the utility of prediction modeling of edentulism.

The future of aging and oral health research must be addressed on multiple fronts, including clinical translation of geroprotective prevention strategies, development of quantitative measures of pace of aging in midlife, and extension of health span by addressing behavioral and social determinants to tackle existing health disparities and reduce the overall burden of age-related disease, enabling access to care at reasonable costs (Sierra et al. 2021). One of the overarching goals is to bring the benefits of geroscience to disadvantaged groups, the people who need it most because they age fastest, die youngest, and are unlikely to participate in clinical trials (Sierra et al. 2021). NIH is continuing to host Geroscience Summits with the fourth held in spring 2023.

D’Souza summarized the NIDCR’s five strategic priorities (NIH, NIDCR 2021a) to advance science along the entire research and workforce spectrum.

Goal 1: Establish the cellular, molecular, behavioral, and environmental determinants that are unique to and shared with other systems.

Goal 2: Develop more precise and individualized ways of managing and preventing dental, oral and craniofacial diseases.

Goal 3: Accelerate the translation of research and the uptake of new discoveries.

Goal 4: Nurture diverse future generations of oral health scientists.

Goal 5: Expand already existing partnerships and create new ones.

All of these goals can be applied to increase oral health equity, diversity, inclusion, and accessibility for our older adults.

Day 3 Discussion

In this session, the discussion touched on many factors involved in addressing the oral health care needs of older adults. These factors include barriers in access to care and the quality of care, as well as new care and workforce models and approaches, taking into consideration associated medical, cognitive, functional, and behavioral challenges within this population. Value-based care, in which prevention is paramount, is being proposed as a care model for older adults, whether institutionalized, homebound, or independently living. However, financial support is needed to initiate and sustain this or other care models and to understand which models are best for older adults in various living situations. Finally, little is known on best methods for improving access, interdisciplinary communication, and collaboration in clinical care for older adults. Individual, community-based, and system-level public health approaches are needed. New technologies and integrated electronic health records across health care systems, including oral health, are opening doors for research using big data. If Medicare included oral health coverage for older adults in an integrated fashion with medical care, this new source of clinical and administrative claims big data would help to identify the best approaches for integrating and improving health care outcomes. The NIDCR is doing its part by supporting research that provides evidence aimed at extending the health span for aging adults.

Discussion

Although we are all aging, some people are more successful at maintaining their health span and longevity than others. These sessions helped us understand geroscience, how the physiologic aging processes work as upstream risk factors for many chronic diseases and conditions. While scientists have traditionally studied one condition at a time, geroscience changes our perspective to view how multiple aging pathways are interconnected and can affect multiple diseases at a time, including those found in the oral cavity.

Aging involves many molecular and cellular pathways that affect the tissues and organ systems throughout the body. They occur in the context of individual, household, and environmental influences; within our myriad health care delivery and finance systems; and in our health policies. Individual susceptibility may be influenced by access to and use of health care, stress, the microbiome, inflammaging, physical activity, cognitive status, diet, nutrition, medications, substance abuse, social isolation, and many other behaviors and exposures. Social, commercial, and environmental determinants of health may accelerate or slow these processes, and these internal and external factors change over time across the life span (Fig. 4). Prevention, intervention, and policy approaches based on aging research are needed to reduce oral and systemic health disparities, support well-being, and prepare for the future health needs of our population.

Figure 4.

Multilevel influences of aging and adult oral health (modified from Fisher-Owens et al. 2007). This model is a depiction of many of the “Aging and Oral Health” topics covered during the 2023 AADOCR Meeting within a Meeting. It is not meant to include all aspects of aging.

The MwM featured DOC and non-DOC experts who discussed the full research spectrum from basic science to public health (Fig. 5). Speakers and the audience during the question-and-answer sessions identified research gaps along with potential solutions and ideas for conducting future research and implementing strategies to advance oral health equity across the older end of the life span.

Figure 5.

Translational science spectrum (NIH, NCATS 2021).

This topic is important because major demographic trends affecting the older adult US population are occurring, including increases in population size, life expectancy, racial/ethnic diversity, socioeconomic disparities, years working, and likelihood of having a disability or chronic disease (NIH, NIDCR 2021b). In the past 2 decades, among Americans aged 65 and older, there has been a dramatic decrease in the prevalence of edentulism from 32% to 17% and an increase in retention of teeth (NIH, NIDCR 2021b). Older people with teeth have very different oral health needs to those who are edentulous. While there are many advantages to maintaining one’s teeth, dentate older adults may become more susceptible to oral diseases if they become unable to maintain their oral hygiene because of physical or cognitive disabilities; have reduced salivary flow due to some chronic diseases, medications, or cancer therapy; or have other medical conditions that affect oral health. Untreated caries for adults ages 65 and older was about 16%, but disparities are present by race/ethnicity and poverty status. Based on the 2011 to 2016 national data, the prevalence was 14%, 29%, and 36% for non-Hispanic White, non-Hispanic Black, and Mexican Americans, respectively, and 33% versus 10% among poor compared to nonpoor older adults. With an increasing prevalence of gingival recession, root caries is also more prevalent among older adults (NIH, NIDCR 2021b).

A broader, upstream perspective, creating a much wider umbrella, highlights the connectedness and synergy among the MwM topics discussed and the placement of oral health conditions (e.g., tooth loss, periodontal disease, dental caries, oral cancer) alongside other health conditions affected by aging such as ADRD, diabetes, aspiration pneumonia, cancer, and cardiovascular disease.

During the first MwM session, the concepts of geroscience and health span, including differences between biologic and chronologic aging, were introduced. Biologic aging pathways, such as stem cell exhaustion and mitochondrial dysfunction (Fig. 2), influence most causes of morbidity and mortality in the United States and developed countries. Geroscience research seeks to understand and influence aging pathways to delay or reverse the aging process, permitting people to live longer without chronic disease and disability. Kaeberlein described research under way in animals using rapamycin that delays the aging process. Some of these mechanisms are also applicable to changes in the oral microbiome, tooth-supporting bone loss, and gingival inflammation leading to periodontal disease. Kirkwood discussed how some of the “hallmarks of aging” described by Kaeberlein, such as cellular DNA damage, cellular senescence, and immunosenescence, can create an environment for inflammaging and tumor development, including oral cancer.

Ryder, during the first session, and Wu, during the second session, discussed ADRD. Upstream, aging processes in the brain may interact with the periodontal pathogen P. gingivalis and gingipain proteases in the development and/or progression of AD and cognitive decline. Wu described epidemiologic studies showing tooth loss and edentulism as important risk factors along this pathway of cognitive decline and subsequent ADRD, with concurrent diabetes as a contributing factor in some age groups (Qi et al. 2021; Jones, Moss, et al. 2023; Wu et al. 2023). These biologic and epidemiologic studies demonstrate the connections among aging processes, oral, and other health conditions.

Cognitive decline may decrease one’s ability to independently maintain oral hygiene. Long-term care residents with ADRD often rely on overworked and undertrained staff to provide their tooth brushing and mouth cleaning. These residents have a high prevalence of oral disease and limited access to comprehensive dental care. Different aging and societal processes may be at work in each direction of oral disease–systemic disease pathways that appear bidirectional (i.e., diabetes and periodontitis relationship). Many biomarkers of initiation of diseases prior to detectable symptoms are yet to be uncovered. They could illuminate the sequence of events and aid in prevention and early detection. The need for collaboration between DOC and non-DOC researchers and different research disciplines is critical. This theme was continued during day 2.

During the second MwM session, the synergies among the topics of loneliness and isolation, nutrition, cognitive decline, and tooth loss in older adults became very apparent during the audience discussion. Perissinotto described the major health effects of loneliness and social isolation. These conditions may be consequences of or risk factors for poor oral health. Touger-Decker discussed how missing teeth, difficulty biting and chewing, and xerostomia may lead to poor diet and malnutrition. Among older adults, eating is often an important social activity. However, impaired ability to eat properly or poor oral esthetics may lead to avoidance of social dining, with the potential for decreasing diet quality and more social isolation and loneliness. Conversely, social isolation, lack of social support, low income, and subsequent medical issues could lead to unhealthy dietary habits, such as cariogenic foods and beverages high in sugar and low in nutrients, malnutrition, and, subsequently, poor oral health.

Causes of malnutrition in older adults with tooth loss remain to be determined. Interprofessional research may help shed light on the many unanswered questions. Does malnutrition lead to tooth loss, or are people with malnutrition more likely to have other conditions that lead to tooth loss? Similarly, there is a lack of research demonstrating whether the changes in diet and poor diet quality lead to tooth loss and how ensuing oral dysfunction results in changes in dietary behaviors and quality. How and whether dietary behaviors, comorbid conditions, sarcopenic obesity, and sociodemographic factors affect the associations between diet, nutrition status, and tooth loss is unknown. There is a dearth of data on how to change the dietary behaviors of older adults with tooth loss. Research in this area would be strengthened by consensus on tools and measures used to assess tooth loss, diet quality, and nutrition status. The effects of functional or ill-fitting dentures and inclusion of dental implants need to be included in studying the interactions among diet, nutrition, tooth loss, and other oral conditions.

Similarly, the relationship between tooth loss and cognitive decline described by Wu may, in turn, be factors associated with social isolation and loneliness. Adults with better cognition may avoid and isolate those less able to communicate effectively or interact properly. Potential partners on dating sites and employers seeking to hire people who need to interact with the public likely prefer adults with a nice smile and good facial esthetics compared to those who do not. Self-rated oral health in research studies is often measured by a 4- or 5-point single-item rating from excellent to poor. The factors most important to older adults in making this determination need investigation. In a community-dwelling sample of older Americans, dentist rating of the older adults’ oral health was significantly higher than the patients’ self-ratings. The variability depended on the patient’s appearance, presence of dry mouth, wearing of a full or partial denture, and current need for dental treatment (Atchison et al. 1993).

These relationships are all ripe for further research to determine the relative strength of different potential causal pathways and associations, as well as to develop and test tailored interventions to improve all of these connected conditions. Common language needs to be used across health care professions, using mutually understood terms such as infection and inflammation. Oral health professionals should be educated, primed, and incentivized to assess loneliness and isolation, as well as other adverse behavioral health conditions, such as substance abuse, depression, cognitive impairment, and poor nutrition in their older adult patients, especially in those who are most vulnerable with missing teeth, poor oral health, and infrequent dental visits. Similarly, health professionals need to be trained to consider the patient’s assessment of their oral health and whether the oral condition is contributing to physical (e.g., pain upon eating) or psychosocial (e.g., refusal to eat with others due to masticatory difficulties) challenges.

During the third MwM session, the focus was on research needed to improve patient care and oral health outcomes for older adults (i.e., to improve the “oral health span” with disease-free and functional oral health throughout life). In the United States, caries prevention programs and health care policies targeting children have started showing success with a reduction in oral health disparities between disadvantaged children and those with more resources (NIH, NIDCR 2021b). Research on caries-preventive agents in older adults demonstrates potential. There have been some studies showing the effectiveness of professionally applied and prescription home-based topical fluorides to prevent root caries (Jones, Gibson, et al. 2023). Silver diamine fluoride has been found to arrest coronal caries in nursing home residents (Shakir et al. 2023) and prevent and arrest root caries in older adults (Hendre et al. 2017). Steps can be taken to change medications, stimulate saliva, and decrease dehydration that result in xerostomia and increase the risk of dental caries (Marchini and Ettinger 2023). However, policies, programs, and funding for improving the oral health of older adults are virtually nonexistent.

A substantial proportion of Medicare beneficiaries have reported chronic oral health issues, including chronic tooth pain and trouble eating solid food due to oral health problems. Only 1 in 3 reported ever having an oral cancer exam (Doss et al. 2020). In the CY2023 Physician Fee Schedule, the US Centers for Medicare & Medicaid Services codified and clarified policies in which Medicare can pay for dental services when that service is integral to treating a beneficiary’s medical condition (e.g., organ transplants, cardiac valve replacements, and valvuloplasty procedures) (CMS 2022). The inclusion of dental benefits in US Medicare Advantage plans varies significantly, resulting in inconsistent coverage. Cost is the most frequently reported barrier to use of dental care, especially among low-income adults over age 65 y (Vujicic et al. 2016). In 2021, 44% of Medicare beneficiaries had no dental coverage (CareQuest Institute for Oral Health 2021). Dental insurance in the United States is primarily employer based.

Large income and racial disparities exist regarding dental utilization among older adults. In the aged population, the long-time separation of dentistry and medicine has become increasingly detrimental and may contribute to undervaluing the oral health of older adults from physical, psychosocial, and quality-of-life perspectives. Perceptions that poor oral health, like wrinkles and hair loss, are ubiquitous in old age as Shakespeare described in the last of the 7 ages of man in the play As You Like It, “sans teeth,” need to be changed.

Ghezzi discussed barriers to access dental care in institutional and home-based settings and recommended that new models are needed for care provision. She emphasized that many barriers to dental care, including a shortage of providers, are a challenge not always found in other aspects of care. A shift to value-based care or other mechanisms that focus on prevention and maintaining health will require changes in provider education, public and private financing, workforce, and delivery mechanisms. Research is needed to determine what new models will improve the oral health span in the most efficacious and cost-effective manner. Mobile dentistry and teledentistry models are helping to reach people who have difficulty receiving care at traditional fixed dental offices. Bringing care to where people are will help increase equitable access to care if professional standards are maintained and financing models are assured. Oral care needs to be better integrated and financed with all other aspects of patient care in institutional and residential settings in an interprofessional manner. After all, much of personal oral health care occurs in the home, not in the dental office.

Slashcheva described the long-term success of Apple Tree Dental in caring for older adults and developing a robust electronic database system available for research. This type of data system is necessary for population-based, longitudinal studies that currently are very limited for studying oral health and oral health care, especially among older adults. Interoperable, interconnected, compatible electronic databases with shared coding across dental and medical care systems are needed for holistic and comprehensive patient care, effective referrals across professions, and research.

Health care systems need to be enabled to address social determinants of health with direct interventions to support needs such as enrollment in Medicaid and Medicare, as well as scheduling and transportation to health care appointments. Social prescribing by health care professionals was described by Perissinotto to address the need for social support to address loneliness, social isolation, dietary behaviors, and vision, hearing, dental, mental, and other functional needs. Research is needed to assess how these interventions address pain, depression, appetite, quality of life, morbidity, and mortality.

Low-cost and conservative treatments for oral health disorders in older persons must be assessed. Service models require development and assessment of their effectiveness, including cost and funding mechanisms. Regarding cost of care, economic and quality of care evidence for expansion of duties by personnel other than dentists (e.g., dental assistants, hygienists, community dental health coordinators, patient navigators, dental therapists, school nurses, long-term care staff) should also be presented to policy makers to demonstrate that costs can be significantly reduced if efficient use of other types of trained personnel are legally allowed, especially in nontraditional settings outside the fixed dental office.

Older adult populations are heterogeneous and experience different life stages and challenges over time. It is important to appreciate these differences when studying oral disease patterns and developing and proposing interventions for the elderly population. Machine learning health systems, advanced informatics, and other technologies are rapidly developing to use big data from biologic systems and omics, electronic health records, and other sources to handle this analytical complexity. With these and other tools, public health researchers and professionals can employ implementation research, as well as evaluate and scale up promising interventions for different communities with different needs.

D’Souza highlighted several studies funded by the NIDCR that link poor oral health in older adults with other systemic conditions and shared the Institute’s goals. Trans-NIH funding opportunities and the NIH Geroscience Summits continue to highlight opportunities and needs for aging research as part of NIH collaborations across institutional centers, including the NIDCR. Although not discussed, potential cross-NIH opportunities could evolve with use of the NIH Common Fund and/or ARPA-H. The NIDCR-funded national dental practice–based research networks and other large-scale public and private clinical programs could include more targeted studies involving dental care for older adults. Similarly, other non–dental practice–based research networks in other disciplines could add oral health status as either risk factors or outcomes in studies of other health conditions such as diabetes, cognitive impairment, and cardiovascular disease.

The need for training oral health personnel to care for aging adults was not discussed but is critical. Most dental students are not provided with sufficient experience in caring for older adults and their wide variety of medical, cognitive, behavioral, and functional needs. Polypharmacy is also common in this population. A review of insurance claims data found instances of dentists prescribing opioids that were inappropriate when combined with certain other medications (Zhou et al. 2020). Generally, dental students are not trained on how to repair a variety of defective restorations. Replacing rather than repairing restorations to provide function raises the cost considerably for patients who can ill afford these expenses. Many practicing clinicians are not comfortable caring for patients who have special needs or need care in a residential or institutional setting outside the dental office. Many of our existing providers need the skills to care for this increasing population. Additional accreditation and continuing education requirements, technologies, and educational research are needed to accomplish this training. Evidence-based decision support tools should also be developed to facilitate chairside decision-making, risk assessment, and treatment planning for older adults with complex medical history and those with limited life expectancy.

Geroscience provides an encompassing framework, rationale, and the necessity for interdisciplinary and interprofessional education, collaboration, patient care, and research. Importantly, aging research across the science spectrum and in every discipline is needed to provide the evidence to drive governmental health policies and funding to develop and implement new solutions to improve our oral and overall health span.

Author Contributions

J.A. Weintraub, contributed to conception and design, data interpretation, drafted and critically revised the manuscript; M. Kaeberlein, C. Perissinotto, K.A. Atchison, X. Chen, R.N. D’Souza, J.S. Feine, E.M. Ghezzi, K.L. Kirkwood, M. Ryder, L.D. Slashcheva, R. Touger-Decker, B. Wu, Y. Kapila, contributed to data interpretation, drafted and critically revised the manuscript. All authors gave their final approval and agreed to be accountable for all aspects of the work.