RELATIONSHIP OF FRAILTY, NUTRITIONAL STATUS AND ORAL HEALTH-RELATED QUALITY OF LIFE IN MEXICO CITY NURSING HOME RESIDENTS

 

M.E. Irigoyen-Camacho¹, M.C. Velazquez-Alva¹, M.A. Zepeda-Zepeda¹, M.F. Cabrer-Rosales¹, I. Rangel- Castillo¹, I. Lazarevich¹, F.R. Barroso-Villafuerte², A. Castaño-Seiquer³, J. Flores-Fraile⁴

 

1. Health Care Department, Metropolitan Autonomous University, Unit Xochimilco, Mexico City, Mexico; 2. Medical Director, Medical Specialty Clinic Virgin of Guadalupe, Mexico City, Mexico; 3. Director of The Master Program of Family and Community Dentistry, Faculty of Dentistry, University of Sevilla, Spain; 4. Dental Clinic Director, Department of Surgery, Faculty of Medicine, University of Salamanca, Spain

Corresponding Author: Maria Consuelo Velazquez Alva, Calzada del Hueso 1100, Col. Villa Quietud, Alcaldía Coyoacán. P.C. 04960, Mexico City, Mexico, Electronic address: mcvelaz@correo.xoc.uam.mx

J Frailty Aging 2023;in press
Published online June 14, 2023, http://dx.doi.org/10.14283/jfa.2023.29

 

---

Abstract

BACKGROUND: We aimed to identify the association among nutritional status, Oral Health-Related Quality of Life (OHRQoL) and frailty, and to estimate the mediation effect of these conditions between age and frailty in a group of Mexico City nursing home residents.
METHODS: We conducted a cross-sectional study. Fried’s phenotype criteria, Full Mini Nutritional Assessment, and General Oral Health Assessment Index was applied.
RESULTS: The participants (n = 286) mean age was 82.4 (± 9.2) years. The prevalence of frailty was 58%, and the prevalence of malnutrition and the risk of malnutrition were 22.7% and 59.5%, respectively. A higher risk of frailty was associated with older age (p = 0.015), sex (women) (p = 0.041), poor nutritional status (p <0.001) and compromised OHRQoL (p <0.001). Approximately 40% of the effect of age on frailty was mediated by nutritional status and OHRQoL (p <0.05).
CONCLUSION: A strong association between nutritional status and frailty was observed. Additionally, OHRQoL was associated with frailty. The effect of age on frailty was mediated by OHRQoL and nutritional status. Interventions targeted to improve nutritional status and oral health may contribute to preventing or delaying the onset of frailty.

Key words: Aging, frailty, malnutrition, nursing homes, oral health.

---

 

Introduction

The number of people aged 80 years and older will reach more than 350 million by the year 2050, and 80% of older adults will be living in low- and middle-income countries (1). In Mexico, in 2019, approximately 15.4 million people were 60 years old and older, which is more than 12% of the county’s population. This proportion is increasing, and by the year 2050, more than 1 in 5 people in Mexico will be over 60 years old (2). The demand for geriatric health services will increase, and the number of those living in nursing homes will probably also increase. Furthermore, the health status of older adults living in this type of residence is generally more compromised than their community-dwelling counterparts, and residents of long-term facilities are frequently care-dependent and have poor nutrition and oral health status (3).
Frailty is a medical syndrome resulting from declining function across multiple physiologic systems. This is a state of increased vulnerability to adverse health outcomes and mortality (4). Frailty is the result of poor homeostasis after external stressors (5). Multiple criteria for the clinical identification of frailty have been proposed; nevertheless, according to Morley (4), most of them are based on a physical deficit model or a specific phenotype model. The Frailty Index is based on the deficit model, which comprises the deficiencies and chronic conditions of the patient, and the physical phenotype model, which is based on five components (undernourishment/weight loss, poor endurance, generalized weakness, unsteady gait, and low/reduced physical activity)(6). The pathophysiologic changes associated with the frailty phenotype have been explored in recent years, and encompass the dysregulation of multiple systems and decreased resilience in frail older adults (7).
Although frailty is considered as an extreme consequence of the normal aging process, age is not the only determining factor for its appearance (8). Frailty and malnutrition are closely related, i.e., a high prevalence of malnutrition has been reported among frail patients and vice versa (9, 10). The simultaneous presence of both conditions is associated with poor quality of life and increased risk of mortality (11). Malnutrition develops slowly, progressively, and silently and is a clinical condition that is highly prevalent in older adults living in nursing homes (12). Additionally, malnutrition is associated with multiple adverse outcomes, such as decreased quality of life, higher health care costs, and increased risk of morbidity and mortality (13). Malnutrition is also associated with tooth loss, impaired chewing ability, and not wearing a dental prosthesis (14, 15). The literature suggests a bidirectional relationship between oral health and nutritional status (16).
Epidemiological studies revealed associations among nutritional status, physical frailty, and oral health. A report of individuals aged 85 or older in Japan and the UK showed a relationship between eating and swallowing difficulties, tooth loss, mobility limitations, and weak handgrip strength. Additionally, in the older adult group in Japan, an association between complete tooth loss and frailty was observed (17).
Azzolino et al. proposed a model to describe the interplay among oral health, nutritional status, and physical frailty. In this model, the relationships between physiological and psychosocial changes are associated with aging. These result in a reduced nutrient intake, and thus, malnutrition leading to physical frailty. Other causes of frailty are chronic diseases and the deterioration of oral health, which can also produce a decline in nutritional status, leading to sarcopenia and physical frailty (18).
The perception of oral health, as evaluated through Oral Health-Related Quality of Life (OHRQoL) instruments, is related to oral health clinical findings in older adults (19, 20). Subjective oral health evaluated using a self-rated oral health question was associated with frailty (21). However, few studies have evaluated OHRQoL dimensions and physical frailty. Motoishi et al. (22) in a cross-sectional study in community-dwelling older adults living on remote islands in Japan identified an association between OHRQoL and physical frailty. Additionally, a cohort study in edentulous older patients of the effect in masticatory ability and OHRQoL found an improvement in the frailty phenotype after rehabilitation with complete dentures (23). However, there is insufficient information on the association between older adult perception of OHRQoL and the occurrence of frailty in other population groups, such as nursing home residents. The identification of these associations could facilitate the inclusion of this type of evaluation when considering the risk factors of frailty. Accordingly, the objective of this study was to identify the association between OHRQoL, nutritional status, and frailty, and to estimate the mediating effect of nutritional status and OHRQoL on age, sex, and frailty in a group of Mexico City nursing home residents.

 

Materials and methods

Desing and participants

A cross-sectional study design was applied in a convenience sample of older adults living in four nursing home residences in Mexico City. We included two nursing homes located in the north and two in the south of the city. The study was performed from November 2018 to February 2019. This study complied with the ethical standards of the Declaration of Helsinki. The protocol was registered by the Council of the Division of Biological Sciences and Health of the Metropolitan Autonomous University and approved by the Institutional Ethics Committee (code: DCBS.CD/ CD.52.17). The objectives and methods of the study were explained to the older adults and their caregivers. Additionally, any questions regarding the study were clarified. Each participant signed an informed consent form agreeing to participate in the study. Participants’ sociodemographic characteristics (date of birth, sex, marital status, and years of schooling) were collected from each nursing home admission file.
The sample size was calculated assuming an odds ratio (OR) between two groups that was different from the null value = 1 (24). Assuming that the odds of frailty in the group with poor OHRQoL were 0.50 and the odds of frailty in the group with good OHRQoL were 0.30, the type one error was set at α =0.05, and the type two error at β =0.20 (power 0.80). The sample size calculated using these figures was n= 192; considering a non-response rate of 20%, the sample size aim was 230 participants. The nursing homes involved had 166 and 186 residents in the north and south, respectively (352 individuals in total). Nursing home authorities requested the evaluation of as many residents as possible.
The inclusion criteria were men or women, 65 years or older, and admission to the nursing home at least six months before the study began. Additionally, to participate in this study, each resident was required to be able to understand and respond to the questionnaires and agreed to receive a nutritional assessment and an evaluation of their handgrip strength.
Health-related records were obtained from the clinical medical history of each participant. Preexisting conditions considered as exclusion criteria were the following: severe cognitive impairment (n =33) according to the results of the Mini-Mental State Examination (score <6) (25), end-stage illnesses (n =10), and those bedridden by chronic or acute disease (n =23). Therefore, the number of excluded residents was 66; out of a total of 352 residents, 286 older adults were included.

Frailty Criteria

The frailty phenotype components described by Fried et al. were used to evaluate frailty status (26); additionally, the adaptation to this criterion by Aguilar-Navarro et al., (27) previously applied in the Mexican Health and Aging Study (MHAS) was implemented Frailty criteria: (1) Unintentional weight loss (>4.5 kg in the last year or Body Mass Index < 22 kg/m2), (2) Exhaustion (During the last two years, have you frequently had severe fatigue or exhaustion?), (3) Low handgrip strength (Mechanical hand dynamometer (TKK 5001; Takei Scientific Instruments, Tokyo, Japan), applying the European Working Group of Sarcopenia in Older People (EWGSOP) cut – off points: <27 kg in men and < 16 kg in women(28), (4) Low walking speed (Because of a health problem, do you experience difficulty walking one block? or because of a health problem, do you have difficulty climbing flights of stairs without resting?), and (5) Low physical activity (During the last two years, have you exercised or done hard physical work on average at least three times a week?). According to the number of affected components, the participants were classified as robust (0), pre-frail (1 – 2), and frail (≥ 3).

Nutritional status assessment

The Full Mini Nutritional Assessment (Full-MNA) was used to evaluate the nutritional status of each participant. This tool has 18 items and its total score ranges from 0 – 30 points. Based on the score obtained, participants were classified as well-nourished (Full-MNA > 24 points), at risk of malnutrition (Full-MNA = 17 – 23.5 points), and malnourished (Full-MNA < 17 points) (29). Anthropometric measurements included in the Full-MNA (weight [kilograms], height [centimeters], calf and mid-upper arm circumferences [centimeters]) were assessed by two registered nutritionists according to recommend standardized procedures (30). A duplicated evaluation was used to assess the examiner’s reliability; the inter- and intra-examiner’s consistency on anthropometric measurements was 97% on a 94%, respectively, in a sample of 31 individuals in whom repeated measurements were performed. Additionally, the Full-MNA items were divided into four components based on Donini et al. (31) classification, (1) medical assessment including mobility, use of prescription drugs, psychological stress, acute diseases, neuropsychological problems and feeding difficulties (seven items with a score range 0 – 11). (2) The second component was anthropometric assessment, body mass index, calf, and arm circumferences, and weight loss during the last 3 months, (four items, score range 0 – 8). (3) Dietary assessment including protein, fruit and vegetables, liquid intake, and the number of meals per day (five items, range 0 – 7), and (4) a subjective component including self-perception of nutritional status and general health status in comparison with other people of the same age (two items, range 0 – 4).

Oral Health-related Quality of Life assessment

To assess OHRQoL the General Oral Health Assessment Index (GOHAI) was applied. GOHAI contains three dimensions, physical function, psychological function, and pain/discomfort. Questions in the physical function dimension include: ‘How often did you limit the kinds or amounts of food you eat because of problems with your teeth or dentures? Also, do you have trouble biting or chewing, or difficulties swallowing?’ Additionally, the instrument contains questions about speech problems. The psychological function dimension includes five items, for instance: limiting contact with people, being worried, concerned, or nervous due to the condition of the teeth or dental prosthesis. Finally, the pain/discomfort dimension asked about the use of medications to treat oral pain, tooth sensitivity with changes in temperature or with sweets consumption, also whether the respondent was able to eat anything without discomfort. This instrument contains a total of 12 items using a Likert scale from 1 (always) to 5 (never), and questions 3 and 7 have inverse values relative to the rest of the items in the instrument. Accordingly, the response codes for these two questions were reversed to describe them and calculate the total GOHAI score. The lowest score is 12 and the highest 60. Higher scores indicate an individual’s better perception of her/his oral health quality of life. The Spanish version of the GOHAI questionnaire, validated in Mexican elderly people (Cohens’ alpha coefficient of 0.77) was used in the current study(32). This instrument contains a total of 12 items using a Likert scale from 1 (always) to 5 (never), and questions 3 and 7 have inverse values relative to the rest of the items in the instrument.

Statistical analysis

The results of quantitative variables are presented as means and standard deviations (± sd), qualitative variables are described as percentages. Logistic regression odds ratios and 95% confidence intervals (95% CI) were obtained for frailty in two categories, those frails, and the pre-frail and normal in another. Four components of the MNA (medical, dietetic, anthropometric, and subjective health assessment) were analyzed in relation to the GOHAI score through a multiple linear regression with robust standard errors. Also, the GOHAI score was dichotomized using the lower quartile value cut-off point. The Full-MNA was dichotomized into a malnourished group and a group at risk of malnutrition, and normal older adults formed the comparison group.
Additionally, generalized structural equation models (GSEM) were built for frailty as the dependent variable, and as independent variables, age, sex, GOHAI, and MNA scores. SEM is a multivariate technique that gives the opportunity to visualize the proposed relationships between variables and includes the estimates of path coefficients (β) indicating the statistical significance of these relationships in the model (33). We applied path analysis, a special case of SEM. In the present study a two-level model was constructed considering that the individuals were nested in their respective nursing homes. The Akaike information criterion was used for model selection. In the mediation analysis indirect and direct effects were obtained using the Buis method (34); total, indirect and direct bootstrapped unstandardized effects were estimated, using 1000 repetitions. Statistical significance was set at α <0.05. The STATA V15 statistical package was used for data analysis (STATA Corporation, College Station, Tx, US).

 

Results

The study included 286 nursing home residents aged 65 and over. The mean age was 82.4 (± 9.2), from 65 to 109 years of age. The number of women was 187 (65.4%), and 99 (34.6%) were men; the mean age was 84.0 (± 8.8) and 79.4 (±9.33), (p<0.001), respectively.
Table 1 presents the sociodemographic characteristics of the participants. 120 (42%) were widowed, approximately one-third (29.4%) were single. The most frequent maximum educational attainment was elementary schooling (42.3%). The residents’ medical history revealed that more than half (57.3%) suffered from hypertension, and 22.0% had type II diabetes mellitus. Table 1 presents the distribution of the residents according to the characteristics that identify the frailty phenotype. The most common feature was low handgrip strength observed in 93.4% of the residents, followed by walking problems or difficulty with stair climbing (60.5%). Only 10 (3.5%) did not meet any of the frailty criteria, and 21 (7.3%) had all five criteria. More than half of the nursing home residents were frail (58.0%), and 38.5% pre-frail. The mean Full-MNA score was 19.81 (±4.26). Based on this instrument, 17.8% of the residents were well-nourished, most of them (59.5%) were at risk of malnutrition, and 22.7% were malnourished.

 

The OHRQoL results showed that the mean GOHAI score was 49.22 (±10.31), the median was 53 (Q1 43, Q3 58). Table 1 presents the percentage of older adults affected in each of the GOHAI three dimensions. The result of each item of the GOHAI score is illustrated in Figure 1. In the physical limitation dimension, difficulties in chewing were experienced by 55.6% of the older adults; in the psychological dimension, worrying about the condition of their mouth was revealed by 46.2% of the participants; and in the pain/discomfort dimension, 38.5% felt discomfort during eating.

How often… Q1: did you limit the kinds or amounts of food you eat because of problems with your teeth or dentures? Q2: do you have trouble biting or chewing any kinds of food, such as tough meat or apples? Q3: were you able to swallow comfortably? Q4: have your teeth or dentures prevented you from speaking the way you wanted? Q5: were you able to eat anything feeling discomfort? Q6: How often did you limit contact with people because of the condition of your teeth or dentures? Q7: were you pleased or happy with the appearance of your teeth and gums, or dentures? Q8: did you use medication to relieve pain or discomfort from around your mouth? Q9: were you worried or concerned about the problems of your teeth, gums, or dentures? Q10: did you feel nervous or self-conscious because of problems with your teeth, gums, or dentures? Q11: did you feel uncomfortable eating in front of people because of problems with your teeth or dentures? Q12: were your teeth or gums sensitive to hot, cold, or sweets? 1. The difficulty/pain/discomfort codes range from always (1) to seldom (4). Coding reversed for Q3 and Q7.

 

The GOHAI index was associated with the MNA score. A high percentage of older adults with poor OHRQoL (GOHAI ≤ 43) (92.6%) were malnourished, and only 7.4% of those with poor OHRQoL were not malnourished (p= 0.004) (Table 2). The odds ratio was 3.52 (95% IC 1.44 8.60), indicating that malnourished residents were more than three times as likely to have poor OHRQoL compared with those who were not malnourished. Consistently, each of the three GOHAI dimensions was independently associated with nutritional status. Older adults who experienced adverse effects on their physical and psychological function or suffered oral pain or discomfort presented higher odds of being at risk of malnutrition/malnourishment compared with their well-nourished counterparts (Table 2).

1. Oral health-related quality of life, 2. Odds ratio calculated using variance–covariance matrix of the estimators by cluster (nursing home), 3. GOHAI quartile 1st cutoff value, 4. at least one negative impact in any item of each GOHAI’s dimension.

 

Table 3 presents the results of the regression model for the MNA components and GOHAI score as dependent and independent variables, respectively. Dietary, anthropometric, and subjective assessments were positively associated with GOHAI score. Considering the score of both dietary and anthropometric assessment also a significant association was observed with GOHAI score (β = 0.056, 95% CI (0.027, 0.085) p= 0.006, R2 =0.107, P= 0.020). The MNA medical assessment component indicated a positive association between OHRQoL and the medical evaluation of the patients. (β = 0.052, 95% CI (0.025, 0.079) p= 0.006, R2 =0.0923, P= 0.023).

1. Regression coefficients adjusted for age and sex, 2. 95% confidence intervals estimated with robust standard errors.

 

To investigate the relationship between hand grip strength and GOHAI score stratified by sex. Regression analyses were conducted in women and men data. In women, better evaluation of OHRQL was associated with a greater strength (β = 0.066, p=0.044) adjusted by age (β = – 0.107, p=0.001. Women with a GOHAI score in the lower quartile had an average grip strength of 8.71 (sd 4.45) while those in the upper quartile had an average grip strength of 11.04 (sd 4.45). Men’s GOHAI scores (β = 0.028, p=0.697) did not show a significant association with hand grip strength.
Table 4 presents the association between sociodemographic characteristics and frailty status is presented in. Being female (OR 1.71, p=0.002) and 80 years old or older was associated with higher odds of being frail (OR 2.27, p=0.031). Marital status and educational attainment were not associated with frailty in the study group. Frail residents were more likely to be affected by their OHRQoL than non-frail or pre-frail participants. (OR = 4.62, p < 0.001) Additionally, Table 4 presents the three dimensions evaluated in the GOHAI instrument by frailty status. Older adults referring at least one negative impact in oral health perception physiological function (OR= 1.72, p =0.033) and in the psychological function dimension (OR= 2.13, p <0.001) were more likely to be frail; additionally, those with pain/discomfort (OR= 2.18, p = 0.023) were approximately twice as likely to be frail.

1. Oral health-related quality of life, 2. Odds ratio calculated using variance–covariance matrix of the estimators by cluster (nursing home), 3. GOHAI quartile 1st cutoff value, 4. at least one negative impact in any item of each GOHAI’s dimension.

 

The results of the mediation analysis are presented in Table 5, including the coefficients of decomposing the total effect of age → frailty. This effect was partially mediated by nutritional status (age → nutritional status → frailty) and by oral health perception status (age → OHRQoL → frailty). Table 4 presents the coefficients of the total, direct and indirect effects by sex. All the coefficients were positive and statistically significant. In women, 39.3% (p=0.003) of the effect of age on frailty was mediated by nutritional status and OHRQOL, and in men, the mediation effect of these variables was 37.8% (p=0.022).

1. Oral health-related quality of life, 2. Unstandardized β coefficients of the effect, 3. bootstrapped unstandardized effects.

 

Figure 2 depicts the directional graph of the structural equation-based path analysis for frailty. A strong association was observed between poor nutritional status and frailty. The frail older adults were more likely to be malnourished compared with non-frail or pre-frail participants (β = 2.60, OR =13.42, p < 0.001). Additionally, participants with poor OHRQoL were more likely to be frail compared with older adults with good OHRQoL (β = 1.43, OR= 4.17, p < 0.001). Women were more likely to be fragile than men (β =0.63, OR= 1.87, p < 0.001).

Coefficient of path analysis (β) *p<0.05, **p<0.01. In the model exogenous variables are assumed to covary.

 

Furthermore, three path analysis models were built, one for each of the three GOHAI dimensions. The results were like those found using the full GOHAI scale (Figure 2). Each of the three dimensions was associated with frailty, independently. The older adults with at least one item affected in oral health perception physical function (β = 0.64, OR =1.90, p =0.034) were more likely to be frail, and comparable results were observed in the psychological function (β = 0.69, OR= 2.00, p 0.020), and pain/discomfort (β =0.61, OR = 1.84, p = 0.033). GOHAI dimensions were associated with frailty.

 

Discussion

OHRQoL was associated with the frailty phenotype in nursing home residents. Each of the three OHRQoL domains—physical, psychological function and oral pain/discomfort—were associated with frailty. Similar results were found in community-dwelling Japanese older adults. In this Japanese cross-sectional study, physical function was associated with frailty, and psychosocial function was associated with the number of frailty phenotype criteria (22). Improving oral health in older individuals may have a favorable impact not only on chewing ability but on other aspects of their lives, increasing their ability to cope with the effects of ageing (23).
Additionally, in the older adults studied, the effect of age on the frailty phenotype was mediated by OHRQoL and nutritional status. These two variables contributed approximately 40% of the effect of age on frailty. Accordingly, in a Canadian nationally representative sample of people aged 45 to 85 years, nutritional status in relation to oral health was identified as having a small but significant mediation effect on frailty (35). In this survey, oral health was evaluated using the self-reported oral health global indicator questionnaire, which requested information regarding specific problems in the previous 6 months, such as toothache, chewing inadequacy, and tooth loss. Almost 50% of participants reported more than two oral health problems. Similarly, in the present study, chewing limitations were mentioned by more than half of older adults.
In Mexican community-dwelling older adults, an association between the perception of poor oral health status and frailty was found (36). In this study, the perception of oral health status was obtained through one question, in which the participants compared their own oral health status with that of people of the same age group. Similarly, in the present study, OHRQoL perception obtained by the GOHAI questionnaire was associated with frailty. This information suggests that the perception of oral health may be a useful indicator of oral health status in the study of the association with frailty (17). Additionally, in this community-dwellers evaluated, old age, female gender, and low utilization of dental services were associated with frailty. In the present study, older people and women were more likely to have poor OHRQoL and be frail. Moreover, in women a significant association between hand grip strength and GOHAI score was observed. Women with a poor OHRQoL were more likely to have low strength. Additionally, periodontitis was associated with low handgrip strength and difficulties in chewing in a longitudinal study in older adults in Finland (37). The reason for this association may be related to the difficulties in eating a good diet when pain, discomfort or inability to chew are present. In men no significant association between GOHAI score and hand grip strength was observed. The gender difference effect could be due to the greater loss of muscle mass observed among women relative to their body weight and hormonal responses.
Oral health is associated with nutritional status (20). Poor oral health in the elderly is characterized by a low number of natural teeth, deficient masticatory function, and a low salivary flow rate. These changes affect dietary habits in older adults, reducing the amount of food consumed. Moreover, foods that are difficult to chew, such as meat, fruit, and vegetables, are frequently substituted by high-carbohydrate food, such as bread and pasta, as they are easy to chew and swallow (20). The association between the MNA medical component and GOHAI indicated that patients with more compromised health status had lower OHRQoL scores. The relationship between general health and oral health has been identified in previous studies (37, 38). This association makes evident the need for a multidisciplinary approach in the care of institutionalized older adults.
In the present study, those nursing home residents with better OHRQoL had better results in the dietary assessment component of the MNA. Wong et al. (20) in a systematic review suggested that the relationship between oral health, OHRQoL, and nutrition in at risk populations warrants exploration. To our knowledge, this is the first study to examine the dietetic and anthropometric components of the MNA and OHRQoL (GOHAI score) in nursing home residents. A relationship was identified between higher frequency in the consumption of fruits and vegetables and better GOHAI score in a population-based cross-sectional study of Japanese older adults (39). In Brazilian adults interviewed in a national survey, an association between feeding difficulties and self-perception of oral health was detected (40). In Malayan adults, an association was found between BMI and OHRQoL (41). MNA is widely used for the evaluation of nutritional status among older adults. This study identified an association of MNA components with OHRQoL. Further studies are required to ascertain the value of these components in the evaluation of the benefits of oral health care interventions.
A Mexican one-year follow-up studied detected higher risk of developing frailty in older adults with poor oral health (42). Accordingly, in a literature review that utilized only longitudinal studies, the association between oral health status and the incidence of frailty was reported. The authors concluded that the accumulation of oral problems, lower number of teeth, low masticatory function, and symptoms of dry mouth were predictors of frailty. It was suggested that further research on the mediating role that nutrition plays in oral health and frailty was required (43). From this perspective, the results of our study support the role of nutrition in the relationship between oral health and frailty.
Very old individuals are more likely to be institutionalized, their health status deteriorates with chronic or acute diseases, and they seldom return to their previous health status (44). Not being able to eat adequately further complicates this scenario. Providing dental care treatment and properly fitted dentures to older adults may improve their quality of life and slow their deterioration (45).
The prevalence of frailty observed in the Mexico City nursing home participants was high, and more than half fulfilled the frailty phenotype criteria. Similarly, through a systematic review and meta-analysis, the estimated pooled prevalence of frailty was 52.3% in nursing home residents (43). Little is known about the prevalence of frailty among older adults living in nursing homes in Mexico. Nevertheless, various studies have been performed in Mexican community-dwelling older adults; a meta-analysis of these reported a prevalence of frailty of 31.2% (46). Similarly, factors associated with frailty, such as advanced age, dependency, and disability, were also associated with nursing home admission (47).
The results of the MNA indicated that 22.7% of participants were malnourished. A similar prevalence (23.4%) was reported in Japanese nursing home residents in a follow-up study of mortality, which applied the MNA-Short form. The authors observed an increased risk of death among malnourished residents based on a 30-month mortality rate adjusted by demographic characteristics and health conditions, thus underlining the importance of nutritional status in nursing home residents (48). An observational study of British residents identified a 41.4% prevalence of malnutrition (10), and an even higher percentage (70.3%) was observed among Spanish adults aged 85 years or older living in nursing homes (49). The discrepancies in the malnutrition prevalence may be explained by residents’ characteristics, such as care dependency and presence of chronic diseases. Furthermore, country-related factors may also influence these differences (50). In the present study, a strong association between nutritional status and frailty was detected. This relationship has been widely described among older community-dwelling and home care older adults in cross-sectional and longitudinal studies from various ethnic groups (9, 10, 51, 52).
Although malnutrition and frailty overlap (53), it is difficult to determine which precedes the other; however, nutrition may have a direct or indirect impact on several of the components proposed to identify frailty according to Fried’s criteria (26). Malnourishment and frailty have a loss of strength and muscle function in common (28). This evidence suggests that a higher energy intake reduces the risk of frailty (54). Similarly, a higher protein consumption and increased physical activity were associated with a reduction in frailty risk (54, 55). Several oral diseases, such as periodontitis or abscess due to untreated dental caries, were linked to chronic low-grade systemic inflammation (56).
The statistical model that we constructed builds on the theoretical model for physical frailty proposed by Azzolino et al., (18) in which the physiological and psychosocial changes related to aging impact nutrient intake. Additionally, when oral health deteriorates, poor nutrient intake develops, which is linked to changes in food selection (17). The GOHAI instrument includes psychological function, and this dimension was independently associated with frailty. The multidimensional aspects of frailty may be affected by oral health perception, e.g., feeling nervous about one’s teeth or limiting social contact due to the status of one’s teeth. These most likely influence the psychological condition of nursing home residents and have a negative impact on frailty (57). The definition of the frailty phenotype applied in the present study was based on the criteria of Fried et al. (26); however, we used the MHAS adaptation of this criteria. In the MHAS sample, 11-year mortality rates were higher in frail individuals as compared with their non-frail counterparts. Additionally, in this sample, the ability to perform instrumental and basic activities of daily living was also associated with frailty (27). Therefore, this definition seems to be adequate for older Mexican adults, and it may be useful in other groups of older adults. Additionally, given the close relationship between frailty and sarcopenia (58), handgrip strength EWGSOP cut-off points were applied to identify low strength in the participants studied (5).
One of the limitations of this study is its cross-sectional design. Additionally, older adults with severe cognitive impairment, terminal diseases, and who were bedridden were not included in the study group. Consequently, the results of the present study cannot be extrapolated to these categories of patients. The participants were gathered from private nursing homes in Mexico City; therefore, the results may not be generalized to older adults in governmental facilities. In Mexico, most nursing homes are private (approximately 85%) (59) , and many are organized by religious groups, as is the case with the nursing homes participants; however, associations between oral health perception quality of life and the oral health status assessed by clinical oral examination have been identified (19, 20). What should we do differently? The poor results in OHRQoL, nutrition, and frailty call for action. In this age group, competing needs may exist, and oral health does not seem to be a priority. However, frequently occurring oral diseases are preventable, and it is possible to grow old with a functional dentition if proper care is provided. The GOHAI questionnaire is considered a gold standard in the evaluation of oral health impact of the geriatric patient (60). It is a simple, fast instrument and may be included as a screening tool to detect frailty in nursing home residents (22).
The further involvement of geriatric physicians with dietitians, dentists, and dental hygienists to provide a multidisciplinary approach may be helpful; the inclusion of a dental hygienist has been recommended to manage oral health in older adults. Additionally, improvements in the regulation of nursing homes and installing comprehensive programs for the elderly are necessary.

 

Conclusions

In conclusion, within the group of Mexican nursing home residents studied, high risks of malnutrition or malnourishment, poor OHRQoL, and frailty were observed. Moreover, a strong association between nutritional status and frailty was observed. Additionally, OHRQoL was associated with frailty. The effect of age on frailty was mediated by OHRQoL and nutritional status. Evaluating the health condition of older adults in nursing home facilities and tailored intervention programs may be a useful strategy to promote functional aging among nursing home residents.

 

Funding: This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.

Author Contributions: Data curation, M.E. I.-C. & M.C.V.-A.; Formal analysis, M.E. I.-C., F.R. B.-V. & M.A. Z.-Z.; Investigation, M.C.V.-A., M.F.C.-R., I. R.-C., & I.L.; Methodology, M.C.V.-A., M.E. I.-C., M.F.C.-R., M. A. Z.-Z., A. & A. C.-S.; Visualization, J. F-F.; Writing – original draft, M.E. I.-C. & M.A. Z.-Z.; Writing – review & editing, M.F.C.-R., I.L, I.R.-C., A. C.-S. & J.F.-F.

Acknowledgments: We want to express our thankfulness to the Doctoral School «Studii Salamantini», Surgery and Odontoestomatoly, University of Salamanca, Spain, for its support in this research.

Ethical approval: Informed consent was obtained from all subjects involved in the study.

Conflicts of Interest: The authors declare that there is no conflict of interest.

 

References

1. World Health Organization. Aging and health-WHO. In 2018. Available from: https://www.who.int/news-room/fact-sheets/detail/ageing-and-health.
2. National Institute of Statistic Geography and Informatics. Statistics on the International Day of Older Persons (October 1) National data [Estadísticas a propósito del día internacional de las personas de edad (1° de octubre) Datos nacionales [Internet]. 2019. Available from: https://www.inegi.org.mx/contenidos/saladeprensa/aproposito/2019/edad2019_Nal.pdf.
3. Papadopoulou SK, Tsintavis P, Potsaki G, Papandreou D. Differences in the Prevalence of Sarcopenia in Community-Dwelling, Nursing Home and Hospitalized Individuals. A Systematic Review and Meta-Analysis. J Nutr Heal Aging. 2020;24(1):83–90.
4. Morley JE, Vellas B, Abellan van Kan G, Anker SD, Bauer JM, Bernabei R, et al. Frailty Consensus: A Call to Action. J Am Med Dir Assoc [Internet]. 2013 Jun;14(6):392–7. Available from: https://linkinghub.elsevier.com/retrieve/pii/S1525861013001825.
5. Cruz-Jentoft AJ, Woo J. Nutritional interventions to prevent and treat frailty. Curr Opin Clin Nutr Metab Care [Internet]. 2019 May;22(3):191–5. Available from: https://journals.lww.com/00075197-201905000-00004.
6. Fried LP, Ferrucci L, Darer J, Williamson JD, Anderson G. Untangling the concepts of disability, frailty, and comorbidity: Implications for improved targeting and care. Journals Gerontol Ser A Biol Sci Med Sci [Internet]. 2004 Mar 1;59(3):M255–63. Available from: https://academic.oup.com/biomedgerontology/article-lookup/doi/10.1093/gerona/59.3.M255.
7. Fried LP, Cohen AA, Xue Q-L, Walston J, Bandeen-Roche K, Varadhan R. The physical frailty syndrome as a transition from homeostatic symphony to cacophony. Nat Aging [Internet]. 2021;1(1):36–46. Available from: http://dx.doi.org/10.1038/s43587-020-00017-z.
8. Gobbens RJJ, van Assen MALM, Luijkx KG, Wijnen-Sponselee MT, Schols JMGA. Determinants of frailty. J Am Med Dir Assoc [Internet]. 2010 Jun;11(5):356–64. Available from: https://linkinghub.elsevier.com/retrieve/pii/S1525861009004113.
9. Barbosa da Silva A, Queiroz de Souza I, da Silva IK, Borges Lopes Tavares da Silva M, Oliveira Dos Santos AC. Factors associated with frailty syndrome in older adults. J Nutr Health Aging [Internet]. 2020;24(2):218–22. Available from: http://www.ncbi.nlm.nih.gov/pubmed/32003414.
10. Fashho E, Ahmed T, Garden G, Readman D, Storey L, Wilkinson L, et al. Investigating the prevalence of malnutrition, frailty and physical disability and the association between them amongst older care home residents. Clin Nutr ESPEN [Internet]. 2020 Dec;40:231–6. Available from: https://linkinghub.elsevier.com/retrieve/pii/S2405457720302011.
11. Kamo T, Takayama K, Ishii H, Suzuki K, Eguchi K, Nishida Y. Coexisting severe frailty and malnutrition predict mortality among the oldest old in nursing homes: A 1-year prospective study. Arch Gerontol Geriatr [Internet]. 2017 May;70:99–104. Available from: https://linkinghub.elsevier.com/retrieve/pii/S0167494317300493.
12. Cereda E, Pedrolli C, Klersy C, Bonardi C, Quarleri L, Cappello S, et al. Nutritional status in older persons according to healthcare setting: A systematic review and meta-analysis of prevalence data using MNA ®. Clin Nutr [Internet]. 2016 Dec;35(6):1282–90. Available from: https://linkinghub.elsevier.com/retrieve/pii/S0261561416000996.
13. Lahmann NA, Tannen A, Suhr R. Underweight and malnutrition in home care: A multicenter study. Clin Nutr [Internet]. 2016 Oct;35(5):1140–6. Available from: https://linkinghub.elsevier.com/retrieve/pii/S0261561415002423.
14. Natapov L, Kushnir D, Goldsmith R, Dichtiar R, Zusman SP. Dental status, visits, and functional ability and dietary intake of elderly in Israel. Isr J Health Policy Res [Internet]. 2018 Dec 10;7(1):58. Available from: https://ijhpr.biomedcentral.com/articles/10.1186/s13584-018-0252-x.
15. Zhu Y, Hollis JH. Tooth loss and its association with dietary intake and diet quality in American adults. J Dent [Internet]. 2014;42(11):1428–35. Available from: http://dx.doi.org/10.1016/j.jdent.2014.08.012.
16. Iwasaki M, Sato M, Yoshihara A, Miyazaki H. Malnutrition and oral disease in the elderly––Is there any bidirectional relationship? Curr Oral Heal Reports. 2017;4(2):70–8.
17. Albani V, Nishio K, Ito T, Kotronia E, Moynihan P, Robinson L, et al. Associations of poor oral health with frailty and physical functioning in the oldest old: results from two studies in England and Japan. BMC Geriatr [Internet]. 2021 Dec 18;21(1):187. Available from: https://bmcgeriatr.biomedcentral.com/articles/10.1186/s12877-021-02081-5.
18. Azzolino D, Passarelli PC, De Angelis P, Piccirillo GB, D’addona A, Cesari M. Poor oral health as a determinant of malnutrition and sarcopenia. Nutrients. 2019;11(12):1–17.
19. Ortíz-Barrios LB, Granados-García V, Cruz-Hervert P, Moreno-Tamayo K, Heredia-Ponce E, Sánchez-García S. The impact of poor oral health on the oral health-related quality of life (OHRQoL) in older adults: The oral health status through a latent class analysis. BMC Oral Health. 2019;19(1):1–10.
20. Wong FMF, Ng YTY, Leung WK. Oral Health and Its Associated Factors Among Older Institutionalized Residents—A Systematic Review. Int J Environ Res Public Health [Internet]. 2019 Oct 26;16(21):4132. Available from: https://www.mdpi.com/1660-4601/16/21/4132.
21. Ramsay SE, Papachristou E, Watt RG, Tsakos G, Lennon LT, Papacosta AO, et al. Influence of poor oral health on physical frailty: A population-based cohort study of older british men. J Am Geriatr Soc. 2018;66(3):473–9.
22. Motoishi Y, Yamanashi H, Kitamura M, Hayashida H, Kawasaki K, Nobusue K, et al. Oral health-related quality of life is associated with physical frailty: A cross-sectional study of Japanese community-dwelling older adults. J Gen Fam Med. 2021;22(5):271–7.
23. Figueredo OMC, Câmara-Souza MB, Carletti TM, Rodrigues Garcia RCM. Chewing ability and oral health-related quality of life in frail elders after new complete dentures insertion: A paired controlled clinical trial. Spec Care Dent. 2020;40(2):168–74.
24. Chow S, Shao J WH. Sample Size Calculations in Clinical Research. 2nd ed. London UK: Chapman & Hall/CRC Biostatistics Series.; 2008. 106 p.
25. Folstein M, Folstein S MchP. Minimental State: a practical method for grading cognitive state of the patients for the clinician. J Psychiatr Res. 1975;12:189–98.
26. Fried LP, Tangen CM, Walston J, Newman AB, Hirsch C, Gottdiener J, et al. Frailty in older adults: Evidence for a phenotype. Journals Gerontol – Ser A Biol Sci Med Sci. 2001;56(3):146–57.
27. Ávila Funes JA, Aguilar-Navarro SG, Amieva H, Gutiérrez-Robledo LM. Frailty among Mexican community-dwelling elderly: a story told 11 years later.The Mexican Health and Aging Study. Salud Publica Mex [Internet]. 2015 Jan 8;57:62. Available from: http://www.saludpublica.mx/index.php/spm/article/view/7591.
28. Cruz-Jentoft AJ, Bahat G, Bauer J, Boirie Y, Bruyère O, Cederholm T, et al. Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing [Internet]. 2019 Jan 1;48(1):16–31. Available from: https://academic.oup.com/ageing/article/48/1/16/5126243.
29. Guigoz Y, Vellas B, Garry PJ. Assessing the nutritional status of the elderly: The mini nutritional assessment as part of the geriatric evaluation. Nutr Rev [Internet]. 2009 Apr 27;54(1):S59–65. Available from: https://academic.oup.com/nutritionreviews/article-lookup/doi/10.1111/j.1753-4887.1996.tb03793.x.
30. World Health Organization. Physical Status: The use and the interpretation of anthropometry. 854th ed. WHO Technical Report Series.; 1995.
31. Donini LM, Stephan BCM, Rosano A, Molfino A, Poggiogalle E, Lenzi A, et al. What are the risk factors for malnutrition in older-aged institutionalized adults? Nutrients. 2020;12(9):1–9.
32. Sánchez-García S, Heredia-Ponce E, Juárez-Cedillo T, Gallegos-Carrillo K, Espinel-Bermúdez C, De La Fuente-Hernández J, et al. Psychometric properties of the General Oral Health Assessment Index (GOHAI) and dental status of an elderly Mexican population. J Public Health Dent. 2010;70(4):300–7.
33. Stephenson MT, Holbert RL, Zimmerman RS. On the Use of structural equation modeling in health communication research. health commun [Internet]. 2006 Jul;20(2):159–67. Available from: http://www.tandfonline.com/doi/abs/10.1207/s15327027hc2002_7.
34. Buis ML. Direct and indirect effects in a logit model. Stata J. 2010;10(1):11–29.
35. Bassim C, Mayhew AJ, Ma J, Kanters D, Verschoor CP, Griffith LE, et al. Oral health, diet, and frailty at baseline of the canadian longitudinal study on aging. J Am Geriatr Soc. 2020;68(5):959–66.
36. Castrejón-Pérez RC, Borges-Yáñez SA, Gutiérrez-Robledo L.M, Ávila-Funes JA. Oral health conditions and frailty in Mexican community-dwelling elderly: A cross sectional analysis. BMC Public Health 2012;12 (1):773. https://doi.org/10.1186/1471-2458-12-773.
37. Hämäläinen P, Rantanen T, Keskinen M, Meurman JH. Oral health status and change in handgrip strength over a 5-year period in 80-year-old people. Gerodontology. 2004;21(3):155–60.
38. Brennan DS, Singh KA. Dietary, self-reported oral health and socio-demographic Predictors of general health status among older adults. J Nutr Heal Aging. 2012;16(5):437–41.
39. Nanri H, Yamada Y, Itoi A, Yamagata E, Watanabe Y, Yoshida T, et al. Frequency of fruit and vegetable consumption and the oral health-related quality of life among Japanese elderly: A cross-sectional study from the Kyoto-Kameoka study. Nutrients. 2017;9(12):1–14.
40. Bordin D, Fadel CB, Moimaz SAS, dos Santos CB, Garbin CAS, Saliba NA. Characterization of the self-perception of oral health in the brazilian adult population. Cienc e Saude Coletiva. 2020;25(9):3647–56.
41. Rosli TI, Chan YM, Kadir RA, Hamid TAA. Association between oral health-related quality of life and nutritional status among older adults in district of Kuala Pilah, Malaysia. BMC Public Health. 2019;19(Suppl 4):1–8.
42. Velázquez-Olmedo LB, Ortíz-Barrios LB, Cervantes-Velazquez A, Cárdenas-Bahena Á, García-Peña C, Sánchez-García S. Quality of life related to oral health in older people. Evaluation instruments. Rev Med Inst Mex Seguro Soc. 2014;52(4):448–56.
43. Hakeem FF, Bernabé E, Sabbah W. Association between oral health and frailty: A systematic review of longitudinal studies. Gerodontology. 2019;36(3):205–15.
44. Kojima G. Frailty as a predictor of disabilities among community-dwelling older people: a systematic review and meta-analysis. Disabil Rehabil [Internet]. 2017 Sep 11;39(19):1897–908. Available from: https://www.tandfonline.com/doi/full/10.1080/09638288.2016.1212282.
45. Ástvaldsdóttir Á, Boström A, Davidson T, Gabre P, Gahnberg L, Sandborgh Englund G, et al. Oral health and dental care of older persons—A systematic map of systematic reviews. Gerodontology [Internet]. 2018 Dec 20;35(4):290–304. Available from: https://onlinelibrary.wiley.com/doi/10.1111/ger.12368.
46. Balcázar JR-, Peña CG-, Solano LF-, Perilla NC-, Sarmiento DSC-, Zepeda MP-. Caregiver burden in caregivers of hospitalized older adults and its associated factors. Geriatr Gerontol Aging [Internet]. 2018 Dec;12(4):196–201. Available from: http://www.ggaging.com/details/493/en-US/caregiver-burden-in-caregivers-of-hospitalized-older-adults-and-its-associated-factors.
47. Gaugler JE, Duval S, Anderson KA, Kane RL. Predicting nursing home admission in the U.S: a meta-analysis. BMC Geriatr [Internet]. 2007 Dec 19;7(1):13. Available from: https://bmcgeriatr.biomedcentral.com/articles/10.1186/1471-2318-7-13.
48. Motokawa K, Yasuda J, Mikami Y, Edahiro A, Morishita S, Shirobe M, et al. The Mini Nutritional Assessment-Short Form as a predictor of nursing home mortality in Japan: A 30-month longitudinal study. Arch Gerontol Geriatr [Internet]. 2020 Jan;86:103954. Available from: https://linkinghub.elsevier.com/retrieve/pii/S0167494319301979.
49. Malafarina V, Serra Rexach JA, Masanés F, Cervera-Díaz MC, Lample Lacasa L, Ollero Ortigas A, et al. Results of high-protein, high-calorie oral nutritional supplementation in malnourished older people in nursing homes: An observational, multicenter, prospective, pragmatic study (PROT-e-GER). J Am Med Dir Assoc [Internet]. 2021 Sep;22(9):1919-1926.e5. Available from: https://linkinghub.elsevier.com/retrieve/pii/S1525861021002978.
50. van Nie-Visser NC, Meijers J, Schols J, Lohrmann C, Bartholomeyczik S, Spreeuwenberg M, et al. Which characteristics of nursing home residents influence differences in malnutrition prevalence? An international comparison of The Netherlands, Germany and Austria. Br J Nutr [Internet]. 2014 Mar 28;111(6):1129–36. Available from: https://www.cambridge.org/core/product/identifier/S0007114513003541/type/journal_article.
51. Setiati S, Soejono CH, Harimurti K, Dwimartutie N, Aryana IGPS, Sunarti S, et al. Frailty and its associated risk factors: First phase analysis of multicentre indonesia longitudinal aging study. Front Med [Internet]. 2021 Apr 29;8. Available from: https://www.frontiersin.org/articles/10.3389/fmed.2021.658580/full.
52. Miettinen M, Tiihonen M, Hartikainen S, Nykänen I. Prevalence and risk factors of frailty among home care clients. BMC Geriatr [Internet]. 2017 Dec 17;17(1):266. Available from: https://bmcgeriatr.biomedcentral.com/articles/10.1186/s12877-017-0660-8.
53. Jeejeebhoy KN. Malnutrition, fatigue, frailty, vulnerability, sarcopenia and cachexia: overlap of clinical features. Curr Opin Clin Nutr Metab Care [Internet]. 2012 May;15(3):213–9. Available from: http://journals.lww.com/00075197-201205000-00004.
54. Schoufour JD, Franco OH, Kiefte-de Jong JC, Trajanoska K, Stricker B, Brusselle G, et al. The association between dietary protein intake, energy intake and physical frailty: results from the Rotterdam Study. Br J Nutr [Internet]. 2019 Feb 28;121(4):393–401. Available from: https://www.cambridge.org/core/product/identifier/S0007114518003367/type/journal_article.
55. Lorenzo-López L, Maseda A, de Labra C, Regueiro-Folgueira L, Rodríguez-Villamil JL, Millán-Calenti JC. Nutritional determinants of frailty in older adults: A systematic review. BMC Geriatr [Internet]. 2017 Dec 15;17(1):108. Available from: http://bmcgeriatr.biomedcentral.com/articles/10.1186/s12877-017-0496-2.
56. Cecoro G, Annunziata M, Iuorio MT, Nastri L, Guida L. Periodontitis, low-grade inflammation and systemic health: A scoping review. Med. 2020;56(6).
57. Freitag S, Schmidt S. Psychosocial correlates of frailty in older adults. Geriatrics [Internet]. 2016 Nov 1;1(4):26. Available from: http://www.mdpi.com/2308-3417/1/4/26.
58. Cesari M, Landi F, Vellas B, Bernabei R, Marzetti E. Sarcopenia and physical frailty: Two sides of the same coin. Front Aging Neurosci [Internet]. 2014 Jul 28;6. Available from: http://journal.frontiersin.org/article/10.3389/fnagi.2014.00192/abstract.
59. Federal Consumer Prosecutor’s Office. Nursing homes. An alternative for the care and attention of the elderly. [Asilos. Una alternativa para el cuidado y atención de los adultos mayores]. [Internet]. 2018. Available from: https://www.gob.mx/profeco/documentos/asilos-una-alternativa-para-el-cuidado-y-atencion-de-los-adultos-mayores?state=published.
60. Winarti TM, Yacob N, Nor W, Wan S, Ali A. The Assessment of quality of life using GOHAI among edentulous patients. J Dent Maxillofac Res. 2019;2(1):1–3.

© Serdi 2023