Abstract
A well-preserved oral function is key to accomplishing essential daily tasks. However, in geriatric medicine and gerodontology, as age-related physiological decline disrupts several biological systems pathways, achieving this objective may pose a challenge. We aimed to make a systematic review of the existing literature on the relationships between poor oral health indicators contributing to the oral frailty phenotype, defined as an age-related gradual loss of oral function together with a decline in cognitive and physical functions, and a cluster of major adverse health-related outcomes in older age, including mortality, physical frailty, functional disability, quality of life, hospitalization, and falls. Six different electronic databases were consulted by two independent researchers, who found 68 eligible studies published from database inception to September 10, 2022. The risk of bias was evaluated using the National Institutes of Health Quality Assessment Toolkits for Observational Cohort and Cross-Sectional Studies. The study is registered on PROSPERO (CRD42021241075). Eleven different indicators of oral health were found to be related to adverse outcomes, which we grouped into four different categories: oral health status deterioration; decline in oral motor skills; chewing, swallowing, and saliva disorders; and oral pain. Oral health status deterioration, mostly number of teeth, was most frequently associated with all six adverse health-related outcomes, followed by chewing, swallowing, and saliva disorders associated with mortality, physical frailty, functional disability, hospitalization, and falls, then decline in oral motor skills associated with mortality, physical frailty, functional disability, hospitalization, and quality of life, and finally oral pain was associated only with physical frailty. The present findings could help to assess the contribution of each oral health indicator to the development of major adverse health-related outcomes in older age. These have important implications for prevention, given the potential reversibility of all these factors.
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Introduction
The last few decades have recorded a number of welcome changes in the global population. Demographic growth and life expectancy are impressive, but population aging is becoming a pressing concern, especially in upper-middle-income countries with a lifespan exceeding 80 years. The main concerns revolve around the quality of the additional years to be lived compared to previous generations; this issue is currently very sensitive [1]. One priority is to better address care challenges posed by older adults while reducing the burden of healthcare resulting from the aging population. As well as improving the overall quality of health in older age, this aim is driving the scientific community to make considerable efforts to develop strategies for the early detection of unhealthy aging phenotypes.
In this respect, deteriorating physical and behavioral functioning is emerging as an increasing burden in long-term healthcare for the aging population. Of greatest concern is the vulnerable subset comprising older adults with multimorbidity, dementia, frailty, and other major adverse health-related outcomes requiring increased care and inducing greater dependency, including hospitalization. Epidemiological evidence suggests that most of these are overlapping, although clinically separate, entities [2]. Indeed, multimorbidity contributes to frailty, functional disability, and increased healthcare costs and also increases the potential for substandard care, given the peculiar treatment setting in clinical practice. Besides, frailty and functional disability accelerate the hazard risk trajectories of adverse health-related outcomes, including mortality.
Oral health is critical to preserving good general health [3]. Geriatric medicine is demonstrating that poor oral health is associated with age-associated physiological burdens, physical frailty [4], sarcopenia [5], cognitive impairment [6], and accumulating multimorbidity [7]. Some biological explanations have been advanced to explain the causal association between poor oral health and age-related physical frailty. The hypothesis of a biological common line between oral health and the different domains of the physical frailty phenotype has been raised. These domains include the functional sphere, through chronic inflammation; the psychosocial aspects, impacting self-esteem and inducing late-life depression (LLD); and the therapeutic approach, involving prevention and damage control [8].
On the basis of these strict links between frailty and oral health indicators, the oral frailty phenotype has been proposed as a conceptualization of age-related gradual loss of oral function, driven by a set of impairments (i.e., loss of teeth, poor oral hygiene, inadequate dental prostheses, difficulty in chewing associated with age-related changes in swallowing) that worsen oral daily practice functions [9, 10]. This novel construct has been defined as a decrease in oral function together with a decline in cognitive and physical functions, as well as possible relationships among oral frailty, oral microbiota, Alzheimer’s disease (AD), and neurodegeneration [11].
Over and above all, poor oral health has a role in driving the risk of hospitalization due to infectious and non-infectious diseases. In this context, the awareness of the risk of developing periodontal disease among individuals with chronic diseases such as diabetes mellitus [12], coronary heart disease [13], respiratory disease [14], and osteoporosis [15] is a recently acquired concept. Indeed, oral infections may be a significant risk factor for systemic diseases, and therefore timely oral health management is critical also to manage non-communicable chronic diseases [16].
All these assumptions, along with the insidious association with survival rates [17], make oral wellbeing a key concept to be preserved, from the preventive and treatment perspective. A large community-based cohort study over a 44-year follow-up demonstrated that number of teeth, marginal bone, and dental plaque were associated with all-cause mortality [18]. Indeed, improving oral health may work well in influencing survival trajectories. Polzer and colleagues demonstrated that treatment of tooth loss protected against mortality [19]. A similar systematic review and meta-analysis revealed that oral care intervention during hospitalization could lead to more favorable mortality-related outcomes [20]. The complex and multidimensional nature of the oral function makes it difficult to clarify its role in affecting adverse health-related outcome trajectories in older age. Therefore, we set up the present systematic review with the aim of summarizing existing evidence about oral health indicators that may be significantly involved in determining a cluster of major adverse health-related outcomes in older age, including mortality, physical frailty, functional disability, quality of life, hospitalization, and falls.
Methods
Search strategy and data extraction
The present systematic review followed the Preferred Reporting Items for Systematic reviews and Meta-Analyses (PRISMA) 2020 guidelines, adhering to the PRISMA 2020 27-item checklist [21]. We performed separate searches in the US National Library of Medicine (PubMed), Medical Literature Analysis and Retrieval System Online (MEDLINE), EMBASE, Scopus, Ovid, and Google Scholar databases to find original articles probing any association between exposure to poor oral health indicator(s) and adverse health-related outcomes in older age. The exposure factors were selected to include any indicator(s) of poor oral health, regardless of the measurement method (clinical examination or self‐reported), and the outcome(s) included major adverse health-related outcomes of aging, i.e., mortality, physical frailty, functional disability, quality of life, hospitalization, and falls. The search strategy used in PubMed and MEDLINE and adapted to the other four electronic sources is shown in Supplementary Table S1. The literature search covers the timeframe from the database inception to September 10, 2022. No language limitation was introduced. Two investigators (VD, ML) searched for papers, screened titles and abstracts of the retrieved articles separately and in duplicate, checked the complete texts, and selected records for inclusion.
Protocol and registration
An a priori protocol was established and registered, without particular amendments to the information provided at registration, on PROSPERO, a prospective international register of systematic reviews (CRD42021241075). Age over 60 years was an inclusion criterion applied when skimming for original papers correlating item(s) referred to poor oral health status and major adverse health-related outcomes linked to the aging process. No skimming was applied to the recruitment settings (home care, hospital, community) or general health status. Technical reports, letters to the editor, and systematic and narrative review articles were excluded.
The following information was extracted by the two investigators (VD, ML) separately and in duplicate in a piloted form: (1) general information about single studies (author, year of publication, country, settings, design, sample size, age); (2) item(s) referred to poor oral health; (3) arbitrarily selected major adverse health-related outcomes in older age (mortality, physical frailty, functional disability, quality of life, hospitalization, and falls). No skimming was applied to assessment methods used to evaluate functional disability and quality of life, while frailty was identified only with the physical frailty phenotype according to the Cardiovascular Health Study (CHS) criteria proposed in 2001 [22] or similar tools or criteria. This choice was driven by a previous systematic review that found 39 articles, when not restricting the search to the most widely used frailty model [8]. The exposure included every oral health indicator measured at least once in the study, regardless of the form of measurement (clinical exam, self-reported). All references selected for retrieval from the databases were managed with the commonly used MS Excel software platform for data collection. Then, all duplicated records were excluded. Potentially eligible articles were identified by reading the abstract and, if warranted, then reading the full-text version of the articles. Data were cross-checked, any discrepancies were discussed, and disagreements were resolved by a third investigator (FP). Lastly, data extracted from selected studies were structured in tables of evidence.
Quality assessment within and across studies and overall quality assessment
The methodological quality of included studies was independently appraised by paired investigators (VD and ML or FP), using the National Institutes of Health Quality Assessment Toolkits for Observational Cohort and Cross-Sectional Studies [23] (National Institutes of Health (NIH), 2018). The ratings high (good), moderate (fair), or poor were assigned to studies according to the criteria stated in the toolkit. This tool contains 14 questions that assess several aspects associated with the risk of bias, type I and type II errors, transparency, and confounding factors, i.e., study question, population, participation rate, inclusion criteria, sample size justification, time of measurement of exposure/outcomes, time frame, levels of the exposure, defined exposure, blinded assessors, repeated exposure, defined outcomes, loss to follow-up, and confounding factors. Items 6, 7, and 13 do not refer to cross-sectional studies and the maximum possible scores for cross-sectional and prospective studies were 8 and 14, respectively. Disagreements regarding the methodological quality of the included studies were resolved through discussion until a consensus was reached, or resolved by a fourth investigator (FL). A modified version of the Grading of Recommendations Assessment, Development and Evaluation (GRADE) rating system was used to assess the overall quality of evidence of the studies included in the present systematic review [24]. The following factors were considered: the strength of association for poor oral health indicator(s) and adverse health-related outcomes, methodological quality/design of the studies, consistency, directedness, precision, size, and (where possible) dose–response gradient of the estimates of effects across the evidence base. Evidence was graded as very low, low, moderate, and high, similar to a GRADE rating system.
Results
The preliminary systematic search of the literature yielded 30,804 records. After excluding duplicates and records removed for other reasons, 2224 were considered potentially relevant and retained for the analysis of titles and abstracts. Then, 1399 articles were excluded for failing to meet the characteristics of the approach or the review goal. After reviewing the full text of the remaining 825 articles, only 68 met the inclusion criteria and were included in the final qualitative analysis (Table 1) [25,26,27,28,29,30,31,32,33,34,35,36,37,38,39,40,41,42,43,44,45,46,47,48,49,50,51,52,53,54,55,56,57,58,59,60,61,62,63,64,65,66,67,68,69,70,71,72,73,74,75,76,77,78,79,80,81,82,83,84,85,86,87,88,89,90,91,92]. The PRISMA 2020 flow chart illustrating the number of studies at each stage of the review is shown in Fig. 1. The endpoints of the literary skimming process resulting in 68 eligible articles evaluating eleven different oral health indicators are listed as follows: masticatory function, tongue pressure, occlusal force, oral diadochokinesis, dry mouth, oral health, periodontal disease, number of teeth, difficulties in chewing, difficulties in swallowing, and tooth or mouth pain (Fig. 2). Given the original heterogeneous labeling, which prevented a rapid conceptual interpretation, we grouped oral health factors into four separate categories: oral health status deterioration (number of teeth, oral health, and periodontal disease); decline in oral motor skills (masticatory function, oral diadochokinesis, occlusal force, and tongue pressure); chewing, swallowing, and saliva disorders (dry mouth, difficulties in swallowing, and difficulties in chewing); and oral pain (tooth or mouth pain).
Preferred Reporting Items for Systematic Reviews and Meta‐analyses (PRISMA) 2020: flow chart illustrating the number of studies at each stage of the review
Eleven oral health items associated to the identified four categories (oral health status deterioration; decline in oral motor skills; chewing, swallowing, and saliva disorders; oral pain), related to six adverse health-related outcomes (mortality, physical frailty, functional disability, quality of life, hospitalization, and falls)
Details of the design (cohort or cross-sectional), sample size (N) and gender ratio (%), minimum age and mean (SD), setting (community, hospital, home care), and country of included studies are shown in Table 1. Given the mixed shape of the recruitment settings for a small percentage of selected studies (2 of the 68), the distribution resulted as follows: 80% (N = 56) community, 17.15% (N = 12) hospital, and 2.85% (N = 2) nursing homes. The Asian continent led the geographical distribution of selected studies (57.14%, N = 40), followed by Europe (28.60%, N = 20, of these 2 studies were from Europe (UK)/North America (USA)), South America (5.70%, N = 4), North America (7.14%, N = 5), and Oceania (1.42%, N = 1) (Figure S1). This latter perspective pointed to both the lack of homogeneity in geographical distribution and the inadequate representativeness of all continents. Mean (SD) age and gender ratio of study participants were recorded if applicable. Across a total of 426,538 subjects, the gender distribution was balanced (48% males versus 52% females). A longitudinal cohort design was more common than cross-sectional (73.5%, N = 50 versus 25%, N = 17); there was only one retrospective study (1.5% N = 1).
Adverse health-related outcomes assessment tools and their distribution across studies
The percentage distribution of the different adverse health-related outcomes investigated in selected studies is shown in Fig. 3. Given the multiplicity of adverse health-related outcomes observed in 5 of the 68 selected studies, in total, 75 outcomes were recorded as the denominator when calculating the representativeness of each adverse health-related outcome. More specifically, three studies were found to simultaneously evaluate two different outcomes each (two of them investigating mortality and functional disability [48, 49], and one investigating hospitalization and mortality [75]), while two studies evaluated three different outcomes, i.e., functional disability, hospitalization, and mortality [65, 66]. Overall, mortality was found to be the most common (38.67%, N = 29 out of 75), followed by physical frailty (29.34%, N = 22 of 65), functional disability (16%, N = 12 of 75), quality of life (8%, N = 6 of 75), hospitalization (5.33%, N = 4 of 75), and falls (2.66%, N = 2 of 75).
Percentage distribution of the different adverse health-related outcomes in older age investigated in the selected studies
As regards the different types of quality of life assessment tools, both the Brazilian validated version of WHOQOL-BREF (25%, N = 2) and the EUROQOL 5D (EQ-5D) (25%, N = 2) were the most frequently adopted, followed by the Short Form 36-Items Health Survey (12.5%, N = 1), the German version of the Philadelphia Geriatric Center Morale Scale (PGCMS) (12.5%, N = 1), the General Life Satisfaction (GLS) (12.5%, N = 1), and the Satisfaction With individual Health status (SWH) (12.5%, N = 1). Of the 6 studies focused on quality of life, one used three different assessment tools [64], while the remaining five each used only one tool [38, 45, 51, 67, 77].
There were 11 studies focused on the functional disability outcome; among them, the most common tool adopted was the certification for Long-Term Care Insurance (LTCI) (50%, N = 6), followed by the Activities of Daily Living (ADL) (16.8%, N = 2), the Functional Independence Measure motor score (FIM) (8.3%, N = 1), the 12-items of behavioral status (8.3%, N = 1), a clinical assessment to evaluate mobility limitations, ADL, and Instrumental Activities of Daily Living (IADL) (8.3%, N = 1), and a single-item questionnaire (8.3%, N = 1), each of which was used only once.
Association among oral health indicators and different adverse health-related outcomes
Mortality was found to be the most studied outcome. We recorded prevailing markers of oral health status deterioration (62.18%), driven by the number of teeth (32.44%, N = 12), followed by the items oral health (16.22%, N = 6) and periodontal disease (13.52%, N = 5) (Fig. 4, panel A). The burden of items belonging to the categories chewing, swallowing, and saliva disorders and decline in oral motor skills was similar (24.32% and 13.5%, respectively). For the chewing, swallowing, and saliva disorders category, the item difficulties in chewing was most frequently associated with mortality (16.22%, N = 6), followed by dry mouth (8.1%, N = 3). For the decline in oral motor skills category, the item occlusal force was most frequently associated with mortality (8.1%, N = 3), followed by masticatory function (5.4%, N = 2) (Fig. 4, panel A).
Doughnut chart for the four categories of oral health items (oral health status deterioration; decline in oral motor skills; chewing, swallowing, and saliva disorders; oral pain), and combined with the corresponding eleven indicators of oral health and relative metrics for each of the heath-related adverse outcomes: mortality (a), physical frailty (b), functional disability (c); quality of life (d), hospitalization (e), and falls (f)
For physical frailty, we recorded prevailing markers of oral health status deterioration (51.04%), driven by the number of teeth (30.62%, N = 15), followed by the items oral health (11.36%, N = 5) and periodontal disease (12.26%, N = 6) (Fig. 4, panel A). For the decline in oral motor skills category, the items masticatory function (8.16%, N = 4) and oral diadochokinesis (8.16%, N = 4) were most frequently associated with physical frailty, while the items tongue pressure (6.12%, N = 3) and occlusal force (6.12%, N = 3) were less common (Fig. 4, panel A). For the chewing, swallowing, and saliva disorders category, the item difficulties in chewing was most frequently associated with physical frailty (8.16%, N = 4) compared to the items dry mouth (6.12%, N = 3) and difficulties in swallowing (4.08%, N = 2). Finally, we found oral pain to be the category least investigated, including only 2.04% (N = 1) of the oral items linked to physical frailty (Fig. 4, panel A).
For functional disability, we found higher representativeness of items of the oral health status deterioration category (66.68%), driven by the number of teeth (46.68%, N = 7), followed by the item oral health (13.34%, N = 2) and periodontal disease (6.66%, N = 1) (Fig. 4, panel A). For the decline in oral motor skills category, the association of the items masticatory function and occlusal force with functional disability was the same (6.66%, N = 1). Finally, for the chewing, swallowing, and saliva disorders category, we found that only the items difficulties in swallowing (13.34%, N = 2) and dry mouth (6.66%, N = 1) were related to functional disability (Fig. 4, panel A).
For quality of life, we identified an overwhelming prevalence of the oral health status deterioration (85.71%) category, driven by oral health (42.86%, N = 2), followed by number of teeth (28.57%, N = 2), and periodontal disease (14.29%, N = 1) (Fig. 4, panel B). The only other category investigated was a decline in oral motor skills (14.29%) covered by the item masticatory function (14.29%, N = 1) (Fig. 4, panel B).
For the hospitalization outcome, each of the categories was represented by a single item, namely oral health (25%, N = 1) for the oral health status deterioration category (25%), masticatory function (25%, N = 1) for the decline in oral motor skills category (25%), and difficulties in swallowing (50%, N = 2) for the chewing, swallowing, and saliva disorders category (50%) (Fig. 4, panel B).
Finally, only two items were found to be associated with falls, the item number of teeth (66.66%, N = 2), representing the oral health status deterioration category (66.66%), and the item dry mouth (33.34%, N = 1), representing the chewing, swallowing, and saliva disorders category (33.34%) (Fig. 4, panel B).
Risk of bias across studies and overall quality of evidence for oral health items associated with adverse age-related outcomes
Examining all 68 included studies, we found a moderate (n=14) to high (n=54) methodological quality (Table 1). An overview of quality ratings within (panel A) and across studies (panel B) is shown in Fig. 5, highlighting areas with higher or lower risk ratings. Bias was detected predominantly in the domains of blinded assessors (detection bias) (68/68 studies, 100% of studies with a higher risk of bias) and sample size justification (selection bias) (66/68 studies, 97% of studies with a higher risk of bias) and, to a lower extent, in the domains of multiple exposure (40/51 prospective/retrospective studies, 78% of studies with a higher risk of bias), participation rate (17/68 studies, 25% of studies with a higher risk of bias), and different levels of exposure (16/68 studies, 23% of studies with a higher risk of bias) (Fig. 5, panel B). Using the GRADE approach, the overall quality of evidence of our four categories was judged moderate for oral health status deterioration; low to moderate for decline in oral motor skills; low for chewing, swallowing, and saliva disorders; and very low for oral pain (Table 2).
Methodological quality assessment within studies (panel A) and overall quality assessment across studies (panel B)
Discussion
The present systematic review explored the relationship between several oral health indicators and their role in determining adverse health-related outcomes including death, physical frailty, functional disability, quality of life, hospitalization, and falls in older age. For the outcome mortality, we recorded prevailing markers of the categories oral health status deterioration; chewing, swallowing, and saliva disorders; and decline in oral motor skills, driven by the items: number of teeth, difficulties in chewing, and occlusal force. For physical frailty, we found associations with indicators of oral health status deterioration (number of teeth), decline in oral motor skills (masticatory function), and chewing, swallowing, and saliva disorders (difficulties in chewing). For functional disability, we found higher representativeness of the oral items number of teeth (oral health status deterioration category), masticatory function/occlusal force (decline in oral motor skills category), and dry mouth (chewing, swallowing, and saliva disorders). For quality of life, we identified an overwhelming prevalence of the oral health status deterioration category driven by the item oral health. The oral item most frequently associated with the hospitalization outcome was difficulties in swallowing for the chewing, swallowing, and saliva disorders category, while only two oral health items were found to be associated with falls, namely number of teeth for the oral health status deterioration category and dry mouth for the chewing, swallowing, and saliva disorders category.
The present findings suggest that the oral health indicator most frequently associated with mortality was the number of teeth. Edentulism is an important oral health indicator in older age [93], capturing cumulative effects of oral diseases over the life course [94]. Worldwide, approximately 30% of adults aged 65–74 years are edentulous, periodontal disease being the primary cause [95]. Recent systematic reviews and meta-analyses have reported reduced survival rates among older edentulous individuals [19, 96, 97]. In particular, in a linear dose–response analysis, Peng and colleagues found 15%, 33%, and 57% increments in the relative risks of all-cause mortality per 10-, 20-, and 32-tooth loss [97]. The present findings also suggest relationships between a reduced occlusal force and higher mortality and between difficulties in chewing and increased survival in older age; these lack previous systematic review/meta-analytical evidence.
Limiting our search to physical frailty, we found an association with indicators of oral health status deterioration, decline in oral motor skills, and chewing, swallowing, and saliva disorders, driven by the items number of teeth, masticatory function, and difficulties in chewing, respectively. In a previous systematic review of all frailty models, we found 12 oral health indicators linked to frailty [8], while another very recent systematic review found 7 oral health characteristics linked to frailty status [4]. Of these oral factors, only three were present in both systematic reviews: number of teeth, difficulties in chewing, and periodontal disease [4, 8]. Two of these three oral items were confirmed in this systematic review focused only on physical frailty, i.e., number of teeth and difficulties in chewing.
For functional disability, we found higher representativeness of the oral items number of teeth for the oral health status deterioration category and masticatory function/occlusal force for the decline in oral motor skills category. For these items, there were no previous systematic reviews/meta-analyses that investigated the relationship with functional disability. We also identified an overwhelming prevalence of the oral health status deterioration category (item oral health) associated with quality of life in older age. In this context, oral health-related quality of life (OHRQoL) is a distinct aspect of health-related quality of life [98]. Together with orofacial pain, orofacial appearance, and psychosocial impact, oral function is one of the four dimensions of the OHRQoL [99]. These four suggested dimensions have been investigated in four very recent systematic reviews [100,101,102,103], suggesting a framework serving to interpret OHRQoL impairment in individual patients, or groups of patients, for clinical practice and research purposes [104]. Previous systematic reviews mainly investigated OHRQoL in specific conditions, or a group of related conditions [103, 105].
A very recent systematic review suggested that OHRQoL in older age predicted global ratings of oral health from 16.4 to 80.2 of variance in relation to the different tools used to evaluate quality of life [106]. The oral items most frequently associated with the hospitalization outcome were difficulties in swallowing/masticatory function, therefore altogether related to oropharyngeal dysphagia, that lack previous systematic review/meta-analytical evidence. Finally, only two oral health items were found to be associated with falls, namely number of teeth (oral health status deterioration category) and dry mouth (chewing, swallowing, and saliva disorders category), again lacking previous systematic review/meta-analytical evidence.
Various possible pathways have been suggested to explain the relationship between oral health and adverse health-related outcomes in older age. In particular, a reduced number of teeth, difficulties in chewing, lower occlusal force/masticatory function, and dry mouth were the oral health indicators most frequently associated with an increased risk of death, physical frailty, functional disability, and falls. The first plausible pathway taking into account these oral indicators and mortality/physical frailty/functional disability/falls is the impact of poor oral health on nutrition, food intake and selection. Among older people with a reduced number of teeth, there is an increased tendency to consume processed food versus raw healthy food, and hence a higher likelihood of inadequate nutrition [19, 107]. Furthermore, the impact of a reduced number of teeth on OHRQoL and multimorbidity [104, 108], may influence the risk of mortality. Nutritional status also appeared to mediate the association between oral health and frailty [110, 111], owing to difficulties in eating. Changes in nutrition intake and malnutrition are also risk factors for dementia and stroke [111, 112]. In particular, tooth loss due to periodontal disease and irregular tooth brushing was associated with a doubled risk of AD [113] and a higher risk of dementia [114]. These diseases and systemic condition such as frailty were the major causes of functional disability in older age. Moreover, there was a cross-sectional association between oral frailty and malnutrition among community-dwelling older adults [59], and the interplay among oral health indicators, nutrition, and frailty supported the novel constructs of oral frailty [8,9,10] and nutritional frailty [110]. In particular, in a very recent Italian population-based study, older people with nutritional frailty, firstly defined as a feature of vulnerable older adults, characterized by loss of weight, muscle mass, and strength (sarcopenia), making individuals susceptible to functional disability [115], were at higher risk for all-cause mortality than those with physical frailty, nutritional imbalance (i.e., two or more of the following: low body mass index, low skeletal muscle index, 58 ≥ 2.3 g/day sodium intake, < 3.35 g/day potassium intake, and < 9.9 g/day iron intake), and cognitive frailty [116]. Moreover, the loss of occlusion due to not using dentures after losing teeth may result in poor functional balance [117], a well-known risk factor for falls [118], and these functional declines may explain the increased risk of falls among subjects with poor dental occlusion. Finally, for the suggested link between dry mouth and falls, a possible underlying mechanism could be that some drugs are associated with dry mouth [119], and patients treated with such medications are more likely to suffer falls [120].
The second possible link of tooth loss to mortality, physical frailty, and functional disability is the inflammatory pathway, where infectious agents, such as Streptococcus sanguinis and Actinobacillus actinomycetemcomitans, play an important role in oral health, possibly exerting direct effects contributing to the pathogenesis of atherosclerosis and thrombosis [121]. On the other hand, periodontal infection/inflammation is a major reason for eventual tooth loss, and tooth loss is a direct marker of a higher level of periodontal inflammation. Therefore, this increasing cumulative inflammation load caused by oral bacterial infections may increase the risk of mortality, in particular due to its adverse impact on the cardiovascular system [30]. A general susceptibility to inflammation with the early onset of inflammation-driven tooth loss or damaged hip or knee joints may also result in higher mortality than in normal populations [122]. Moreover, a relationship between inflammation and frailty has been suggested [123], and the inflammatory status may increase oxidative stress and insulin resistance, reducing the muscle capacity to synthesize proteins [124], thereby increasing the risk of functional disability in older age.
Difficulties in chewing and lower occlusal force/masticatory function were other oral health predictors associated with mortality, physical frailty, and functional decline identified in the present systematic review. At present, only one operational definition of oral frailty has been introduced, by Tanaka and colleagues [59], based on the identification of six oral health items (i.e., number of teeth, masticatory function, difficulties in chewing, oral diadochokinesis, tongue pressure, and difficulties in swallowing) showing an increased risk of physical frailty, sarcopenia, functional disability, and all-cause mortality. The first three oral items suggested by this operational definition are among the indicators mostly identified in the present systematic review (i.e., number of teeth, masticatory function, and difficulties in chewing). Another possible definition of oral frailty was that encompassing difficulty in chewing associated with age-related changes in swallowing (presbyphagia) [8,9,10]. Therefore, sarcopenia, a progressive and generalized skeletal muscle disorder involving the accelerated loss of muscle mass and function, could be the connecting link, possibly describing a novel frailty phenotype. To date, sarcopenia is recognized as a whole-body process also affecting masticatory and swallowing muscles (sarcopenic dysphagia) [125]. A reduced nutrient intake in older individuals is directly or indirectly associated with a progressive loss of muscle mass and a decline of oral functions, and coordination capabilities, all of which partly or jointly affect the intricate process of swallowing/eating [126]. With links to both oral frailty and nutritional frailty [8, 100], sarcopenia could share a bidirectional relationship with cognition, producing muscle dysfunction, slow gait, and cognitive dysfunction [127, 128]. Furthermore, the oral health indicators most frequently associated with the hospitalization outcome (i.e., difficulties in swallowing/masticatory function) also encompassed the conditions oropharyngeal dysphagia/sarcopenic dysphagia. Finally, sarcopenia may also be an underlying factor explaining the oral health-falls link because it can cause both swallowing disorders and an increased risk of falls [120].
The link between poor oral health and adverse health-related outcomes may also have some underlying psychosocial factors that should be explored. For example, the social effects of oral health deterioration and its impact on OHRQoL [129], given that loneliness could contribute to the development of frailty [130], mortality [131], and functional disability [132]. However, in older age, for the link between oral health indicators and OHRQoL, we must also take into account the other three dimensions (i.e., orofacial pain, orofacial appearance, and oral function) to better interpret OHRQoL impairment in specific groups of patients [104]. Finally, LLD may affect mortality [133], frailty [134], functional disability [135], OHRQoL [136], hospitalization [137], falls [138], and oral health status [139]. In particular, LLD is frequently associated with poor oral hygiene, a cariogenic diet, diminished salivary flow, rampant dental decay, advanced periodontal disease, and oral dysesthesias [139].
In the present systematic review, owing to the heterogeneity of different variables in oral health assessment and the evaluation of the different adverse health-related outcomes, a quantitative meta-analysis might be unreliable. Some other limitations of the present systematic review should also be considered. Firstly, the study designs were different in the selected studies. The statistical survey of oral factors associated with different adverse health-related outcomes, even using the same definition, was different among the studies, in terms of the rating tools used and the definition of the oral items. Secondly, the number of oral items and the sample size varied between studies. Given the original heterogeneous labeling, we subjectively grouped oral health indicators in four separate categories, driven by the oral health items found in the reviewed studies, with some degree of overlap between these categories (i.e., deterioration of oral motor skills and chewing, swallowing, and saliva disorders).
Conclusion
The present systematic review highlights the importance of oral health as a predictor of several adverse health-related outcomes in older age and shows that the use of oral health indicators in health surveys and clinical practices when conducting a comprehensive clinical oral examination is not currently adequate. In fact, oral health is a part of an individual’s general health status, and a multidisciplinary approach is needed to assess the contribution of oral health measures to specific conditions. On May 27, 2021, the World Health Assembly passed its first-ever resolution on oral health, recognizing it as an issue of global concern, and urging member states to address causes of oral disease, particularly as they overlap with other non-communicable diseases (diets with a high sugar and alcohol content, a smoking habit), and to enable better access to dental care [140]. The number of teeth may serve as a good marker for general health, reflecting the net accumulation of experiences over time, from poor hygiene habits to the occurrence of caries, periodontal diseases, and trauma. Furthermore, routine oral health assessment could pose several challenges in non-gerodontologic settings. In fact, dentists’ conceptions of good healthcare were in line with the conceptualization of patient-centered care; however, inadequate reimbursement and limited resources and time were the most important barriers to providing good care, while one of the most important facilitators was healthcare providers’ attitude and motivation [141]. The tooth count is clinically friendly information that can be easily retrieved during the comprehensive geriatric assessment (CGA) of older people. This oral health indicator may provide useful insights supporting the design of the most appropriate intervention, i.e., the maintenance and/or improvement of oral function and nutritional status. In the near future, oral deficits could be used to integrate the CGA, so as to measure the contribution of oral diseases to frailty and other adverse health-related outcomes in older age. Maintaining or increasing oral function may be associated with an improvement of dietary and functional status in older people and may be implicated in reducing the risk of mortality and of the development of frailty and other major adverse health-related outcomes.
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Acknowledgements
We thank the “Salus in Apulia” Research Team. This manuscript is the result of the research work on frailty undertaken by the “Italia Longeva: Research Network on Aging” team, supported by the resources of the Italian Ministry of Health—Research Networks of National Health Institutes. We thank M.V. Pragnell for her precious help as native English language supervisor. All authors have access to all the data reported in this systematic review.
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VD and FP conceptualized this systematic review. ML, RS, AB, GB, AM, HJC-J, GDP, RS, AD, and ADa contributed to data collection. VD, FL, RS, ML, MP, FS, VS, DM, and FP contributed to data interpretation. All authors contributed to drafting, revising, and approving the submitted paper.
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Dibello, V., Lobbezoo, F., Lozupone, M. et al. Oral frailty indicators to target major adverse health-related outcomes in older age: a systematic review. GeroScience 45, 663–706 (2023). https://doi.org/10.1007/s11357-022-00663-8
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DOI: https://doi.org/10.1007/s11357-022-00663-8