Oral Frailty and Its Association with Cognitive Function and Muscle Strength in Patients on Maintenance Hemodialysis: A Retrospective Observational Study

Abstract

Background: Oral frailty is a new concept, introduced in Japan in 2013. In our preliminary study, oral hypofunction was observed in more than half of patients undergoing maintenance hemodialysis (MHD). This allowed us to determine the exact prevalence of oral frailty in MHD patients and investigate the association between oral cavity function, findings obtained via comprehensive geriatric assessment, and motor features. Methods: We initiated a two-week hospitalization program for MHD patients to evaluate frailty including oral cavity functions. Along with a comprehensive geriatric assessment and evaluation of motor functions, seven items pertaining to oral cavity functions were assessed by a professional dentist to determine oral frailty. After the incidence of each item had been determined, the association between these factors was retrospectively analyzed to explore the factors that affect oral frailty. Results: Oral frailty was observed in 33 out of 50 patients (66%). In particular, tongue lip motor functions were frequently impaired in this population. Oral cavity function scores, which increased as oral function deteriorated, negatively correlated with cognitive function (r = −0.349; p = 0.0129; 1−β = 0.71) and grip strength (r = −0.364; p = 0.00933; 1−β = 0.75). Conclusions: Oral frailty was commonly observed in MHD patients. We are currently considering implementing exercise programs to improve tongue lip motor function, enhance cognitive function through interprofessional cooperation, and strengthen grip.

1. Background

Oral frailty was first described by the Japanese Society of Gerontology in 2013 and was defined as a decline in oral function accompanied by a decrease in cognitive and physical functions [1,2]. The major causes of oral frailty include poor dental status and sarcopenia [3]. Oral hypofunction is defined as the presentation of seven oral signs or symptoms: oral uncleanliness, oral dryness, reduced occlusal force, impaired tongue and lip motor function, decreased tongue pressure, diminished chewing function, and impaired swallowing function [4]. The criteria for each symptom were determined based on the data from previous studies. According to Japan Dental Association, the presence of more than three symptoms constitutes a diagnosis of decreased oral function, corresponding to the third stage of oral frailty [4,5]. Patients undergoing maintenance hemodialysis (MHD) are known to be susceptible to infection, which accounts for approximately 23% of all deaths [6]. Almost half of the deaths caused by infections in patients on MHD are caused by pneumonia. Decreased oral function is associated with susceptibility to respiratory infectious diseases, as well as with their severity.

Shinseikai Dai-ichi Hospital is located in the eastern part of Nagoya City and has 144 hospital beds and 100 dialysis beds. Our hospital belongs to the HOSPY group, which comprises our hospital, one acute-care hospital, and six outpatient dialysis clinics. We have approximately 1400 patients undergoing hemodialysis. Given that the average age of hemodialysis patients is 73.3 years old, instrumental activities of daily living (IADLs) are frequently reduced and a decline in muscle strength is commonly observed. We conducted a preliminary survey of oral cavity function in outpatient dialysis patients and found that oral hypofunction was recognized in 57 out of 86 patients. We then determined the exact prevalence of oral frailty in MHD patients and investigated the association of oral cavity function with findings obtained via comprehensive geriatric assessment (CGA) [7] and motor features to explore the factors affecting oral frailty in MHD patients.

2. Methods

2.1. Study Design and Participants

In October 2023, we initiated a two-week hospitalization program for MHD patients (Frailty Measures Hospitalization) to evaluate frailty, including motor features and oral cavity functions, and to investigate the risk of cardiovascular diseases and other organic diseases (Figure 1). The criteria for Frailty Measures Hospitalization included patients undergoing hemodialysis who were willing to participate in the program and who could walk independently. Our preliminary survey on oral frailty revealed that the prevalence of oral frailty did not differ significantly between the individuals aged less than 65 years (n = 10) and aged 65 years older (n = 76). Impaired tongue lip motor functions were commonly observed in both groups (Tenma M, unpublished data). Accordingly, all of the consecutive MHD patients who participated in the program were enrolled in this study.

2.2. Comprehensive Geriatric and Motor Assessment

The CGA was performed on admission using the TMIG index of competence, Geriatric Depression Scale (GDS) 15, Vitality Index, and Hasegawa’s Dementia Scale-Revised (HDS-R). Motor functions were evaluated by measuring grip strength, leg muscle strength, and calf circumference, using a short physical performance battery (SPPB) and AI gait analysis. In addition, a two-step test was performed to determine the degree of locomotive syndrome (severe; 0.9>, mild; 0.9 or above and below 1.3, robust; ≥1.3).

2.3. Oral Cavity Function Assessment

During admission, seven oral cavity function items were assessed by a professional dentist (Figure 2). In our analysis, oral frailty was defined as obtaining a poor result in ≥3 of the 7 measures. The degree of tongue coating was assessed via visual inspection using the Tongue Coating Index (TCI). A TCI score of 50% or higher was used to diagnose poor oral hygiene. An oral moisture checker was used to measure mucosal wetness. Oral dryness was defined as a moisture level below 27.0 as measured using the oral moisture checker. When the number of natural teeth, excluding the remaining roots and teeth with grade 3 mobility, was less than 20, a diagnosis of reduced occlusal force was made. Tongue lip motor function was evaluated by counting the number of oral diadochokinesis (OD) syllables (pa, ta, and ka) produced per second. Oral dysdiadochokinesis was diagnosed when the oral diadochokinetic rate of any of the syllables was <6.0. Subsequently, the incidence of each item was determined.

2.4. Statistical Analysis

Retrospective observational study was performed. Data were analyzed using descriptive statistics. The results of the stratified analysis were compared between two groups using Fisher’s exact test or the Mann–Whitney U test. Correlation analysis was performed using Spearman’s rank test with logistic regression analysis. All p-values were two-sided, and p-values of 0.05 or less were considered statistically significant. Statistical analyses were performed using EZR (Saitama Medical Center, Jichi Medical University, Saitama, Japan), which is a graphical user interface for R (The R Foundation for Statistical Computing, Vienna, Austria). Specifically, it is a modified version of the R commander, designed to add statistical functions frequently used in biostatistics [8]. In addition, to evaluate the statistical power as determined by (1−β) for the correlation results, a post hoc power analysis was performed using G*Power (version 3.1.9.7; Heinrich Heine University Düsseldorf, Düsseldorf, Germany) [9]. This study was approved by the Ethics Committee of Shinseikai Dai-ichi Hospital (S2023-#011), approved date: 3 February 2024.

3. Results

3.1. Baseline Characteristics and Oral Hypofunction

We enrolled consecutive 50 patients on MHD who had been hospitalized for frailty measures as of 15 April 2025. The patient demographic characteristics are listed (

Table 1. Demographic features.

	Total	Male	Female
Gender	50	35	15
Age (yr); median (range)	77.5 (37–90)	77 (37–90)	79 (49–90)
History of hemodialysis (months); median (range)	94.5 (5–266)	87 (7–246)	122 (5–266)
Basic disease
Diabetic kidney disease	28	21	7
Nephrosclerosis	13	10	3
Nephritis	5	3	2
Others	4	1	3

). IADL values, determined based on the TMIG index of competence were often reduced in MHD patients and, in particular, the aspect of social roles was impaired in approximately 80% of MHD patients (

Table 2. Comprehensive geriatric assessment.

	TMIG Index of Competence
	Total	Instrumental	Intellectual	Social
Full	15%	35%	42%	19%
Decreased	85%	65%	58%	81%
Geriatric Depression Scale 15		Vitality Index		HDS-R
10≤: depression	15%	Full	77%	20≥: cognitive decline	19%
10>	85%	Decreased	23%	20<	81%

). Oral hypofunction with three or more positive signs or symptoms was observed in 33 out of 50 MHD patients (66%) (

Table 3. Oral cavity function.

		Number	Prevalence
Oral frailty		33	66%
1	Plaques/tongue coating	35	70%
2	Dry mouth test	7	14%
3	Occlusal forces	24	48%
4	Tongue-lip motor function	50	100%
	pa	44	88%
	ta	45	90%
	ka	50	100%
5	Tongue pressure test	25	50%
6	Chewing ability test	14	29%
7	Swallowing (EAT-10)	4	8%

). TCI was increased in 35 patients (70%), and the number of OD syllables was decreased in all patients [pa 44/50 (88%), ta 45/50 (90%), ka 50/50 (100%)] compared to the standard range, whereas dry mouth was observed in only 7 cases (14%).

3.2. Associations among Oral Function, Cognition and Motor Performance

The number of OD/pa/syllables correlated with the TMIG index of competence (p = 0.0325). Moreover, the number of OD/pa/ / ta/ / ka syllables was significantly positively associated with HDS-R scores (r = 0.442; p = 0.00131; 1-β = 0.91, r = 0.376; p = 0.00715; 1-β = 0.78, r = 0.291; p = 0.0404; 1-β = 0.55) (Figure 3). Oral cavity function scores, which increased as oral function deteriorated, were negatively correlated with cognitive function as measured using the HDS-R (r = −0.349; p = 0.0129; 1-β = 0.71) (Figure 4).

As for motor function, grip strength decreased in 46 (male; 34/35, female; 12/15) out of 50 MHD patients (

Table 4. Motor features.

		Total (n = 50)	Male (n = 35)	Female (n = 15)
Decreased grip strength	Number	46	34	12
Male < 28 kg; Female < 18 kg	Prevalence	92%	97%	80%
Locomotive syndrome	Number	45	32	13
Two-step test < 1.3	Prevalence	90%	91%	87%
Short physical performance battery (SPPB)	Number	18	13	5
8≥	Prevalence	36%	37%	33%
AI analysis of gait	Number	25	18	7
16≥	Prevalence	50%	51%	47%

), and oral cavity function scores correlated negatively with grip strength (r = −0.364; p = 0.00933; 1-β = 0.75) (Figure 5). Locomotive syndrome was evident in 45 cases (male; 32/35, female; 13/15) as shown in Table 4. The prevalence of oral frailty was 71% (32/45) and 20% (1/5) in MHD patients with and without locomotive syndrome, respectively, which was significantly different (Fisher’s exact test; p = 0.004). In contrast, oral dysdiadochokinesis was present in all patients on MHD, regardless of the presence or absence of locomotive syndrome (

Table 5. Association between oral frailty and locomotive syndrome.

	Total	Oral Frailty +	Oral Frailty −	Oral Dysdiadochokinesis	pa	ta	ka
Robust	5	1 (20%)	4 (80%)	5 (100%)	4	5	5
Locomotive syndrome	45	32 (71%)	13 (29%)	45 (100%)	40	40	45
Mild 0.9–1.3	21	16	5	21	17	18	21
Severe 0.9>	24	16	8	24	23	22	24
Total	50	33 (66%)	17 (34%)	50 (100%)	44	45	50

).

4. Discussion

Oral frailty is a relatively new concept that was introduced in Japan in 2013 [2,4]. So far, researchers have defined oral frailty in different ways and there is no consensus on the relationship between oral frailty and oral hypofunction [10]. Oral frailty has been reported to be associated with declines in mental and physical function [1,2,3,11], suggesting that it should be identified using a variety of methods [3,11,12]. Given our belief that a detailed diagnosis of oral frailty should include dental evaluation, oral hypofunction determined by dentists was considered the third level of oral frailty [4,5] in the current study. Our retrospective observation demonstrated that the prevalence of oral frailty based on our definition was 66% (33/50) among MHD patients, which was much higher than that among community-dwelling elderly individuals (19.3–24%) [12,13] and elderly hospitalized patients (31.0%) [13]. Oral frailty was previously reported to be significantly associated with 2.4-, 2.2-, 2.3-, and 2.3- fold increased risk of physical frailty, sarcopenia, disability, and mortality, respectively [5,14]. The recovery and maintenance of oral function should help extend healthy life expectancies. We found that oral hypofunction, the third level of oral frailty, was closely related to cognitive function and grip strength.

Oral frailty Index-8 (OFI-8) is an eight-item screening questionnaire designed based on the results of the Kashiwa study to identify adults who may be at risk of oral frailty [15]. The OFI-8 includes key indicators of oral frailty, such as oral health-related behaviors, social participation, denture use, and chewing ability. Its convenience and comprehensiveness make it a useful screening tool. Although the OFI-8 is commonly used to detect oral frailty, it lacks objective indicators. In the current study, seven oral cavity function items were assessed, and the diagnosis of oral hypofunction was made by a professional dentist to overcome this drawback of the OFI-8.

Tongue coatings are frequently observed in patients on MHD. This poor oral hygiene might be explained by patients struggling to visit the dentist regularly because they needed to undergo hemodialysis treatment three times a week. Oral dryness occurred less frequently than expected in this study. The prevalence of xerostomia was previously reported to be 52.3% among patients on MHD [16], which could be due to daily fluid restriction and the aging-related atrophy of saliva glands causing dry mouth. This discrepancy may be explained by the fact that our enrolled patients were hospitalized for frailty measures, and fluid management can be easily performed in a hospital setting compared with outpatient dialysis. Additionally, oral function was assessed at admission, prior to hemodialysis treatment, which may have influenced the findings.

Among the seven items examined in relation to oral cavity function, oral dysdiadochokinesis was notable in MHD patients. The number of OD/pa// ta// ka syllables per second, especially pa, had a significantly positive correlation with the scores for the HDS-R and TMIG index of competence. In general, OD/pa is used to evaluate lip movement, whereas OD/ta and OD/ka are used to assess the motion of the anterior and posterior regions of the tongue [4]. OD/pa yielded the highest statistical power among the three syllables in post hoc analysis, suggesting the strongest correlation between OD/pa and cognitive function. The orbicularis oris muscle plays an important role in pronouncing the syllable/pa along with eating and swallowing. Therefore, a decreased OD/pa reduces the labial closure force and impairs the oral stage of swallowing. Miura et al. previously reported that labial closure force is significantly related to HDS-R scores and IADL [17], which is consistent with our present findings. In addition to oral dysdiadochokinesis, decreased oral function and a third level of oral frailty were observed more frequently in patients with locomotive syndrome than in those without it. In addition, decreased grip strength is strongly associated with oral hypofunction, and it is necessary for patients on MHD to improve their muscle strength.

A recent prospective cohort study on hemodialysis patients showed that the oral frailty group had a significantly higher proportion of patients with worsening nutritional status and sarcopenia during one-year follow-up [18]. Oral frailty causes a reduction in food intake and dietary diversity, leading to malnutrition. Malnutrition contributes to the progression of sarcopenia, and the weakening of the muscles around the mouth can exacerbate oral frailty. This vicious cycle worsens oral frailty in patients undergoing MHD who are prone to sarcopenia. Furthermore, patients on MHD usually eat alone, with few social interactions, especially during meals. In fact, there are a number of individuals among our patients on MHD who live alone. Even when patients live with their families, hemodialysis usually continues until late in the afternoon, and so they often eat alone, later. According to our CGA findings, social frailty is usually present in patients undergoing MHD. Among community-dwelling older adults, eating alone is significantly associated with oral frailty [13]. It is crucial for patients on hemodialysis to improve their eating habits and encourage social participation through interprofessional cooperation, which includes family, corporations, local governments, and the medical community [1,5,19]. The MHD patients enrolled in the current study had fairly good ADL and walked on their own; nevertheless, oral frailty was detected in more than 60% of them. Accordingly, the prevalence of oral frailty among MHD patients is suspected to be exceedingly high compared to that among community-dwelling elderly individuals. Oral frailty may be considered as a “diseasome” [20] that encapsulates the complexity and interconnectivity of biological factors, because this condition can lead to a variety of associated diseases. Network-based approaches are necessary in the prevention of oral frailty among patients on hemodialysis, to allow them to live a healthy, happy, and long life.

This study had several limitations. Firstly, the present findings were obtained from a single institute and the sample size was very small. Therefore, post hoc analyses were conducted using G*Power to evaluate the statistical power of the results of our association analysis. Although the statistical power was not sufficient (1−β ranged from 0.71 to 0.91), we do believe that our results may be clinically relevant, given the constraints of the target population. Secondly, this was a retrospective observational study and not a randomized controlled trial. To define oral frailty, we applied seven items of oral cavity function, whereas most studies use subjective methods, including the OFI-8 [3,10,18]. The prevalence of oral frailty may have been overestimated in this study. Thirdly, in the present analysis oral cavity functions were evaluated by a single dentist. Although the results might be affected by risk of bias during assessment of oral frailty, each item of oral cavity functions was essentially determined in an objective way. It is less likely that examiners calibration should be considered. Fourthly, confounding factors such as medications, dietary habits, education level, and sleep quality cannot be neglected when interpreting the data obtained [1,2,3,10,21]. To exclude the effects of hemodialysis, oral cavity function was evaluated before hemodialysis. Finally, we did not obtain basic data on the underlying mechanisms linking oral frailty, cognitive function, and grip strength.

5. Conclusions

Based on the present findings, we decided to instruct patients on MHD to perform oral exercises aimed at improving tongue lip motor function. In addition, we are currently considering implementing exercise programs to enhance cognitive function through interprofessional cooperation and increase grip strengthen during the Frailty Measures Hospitalization intervention. It is also important to maintain optimal oral hygiene levels by conducting regular dental checkups.