Abstract
Background
Aging anorexia, defined as loss of appetite and/or reduced food intake, has been postulated as a risk factor for frailty. Impairments of taste and smell perception in elderly people can lead to reduced enjoyment of food and contribute to the anorexia of aging.
Objective
To evaluate the relationship between frailty and taste and smell perception in elderly people living in urban areas.
Design
Data from the baseline evaluation of 768 residents aged ≥ 65 years who enrolled in a comprehensive geriatric health examination survey was analyzed. Fourteen out of 29-items of Appetite, Hunger, Sensory Perception questionnaire (AHSP), frailty, age, sex, BMI, chronic conditions and IADL were evaluated. AHSP was analyzed as the total score of 8 taste items (T) and 6 smell items (S). Frailty was diagnosed using a modified Fried's frailty criteria.
Results
The area under the receiver operator curves for detection of frailty demonstrated that T (0.715) had moderate accuracy, but S (0.657) had low accuracy. The cutoffs, sensitivity, specificity and Youden Index (YI) values for each perception were T: Cutoff 26.5 (YI: 0.350, sensitivity: 0.639, specificity: 0.711) and S: Cutoff 18.5 (YI: 0.246, sensitivity: 0.690, specificity: 0.556). Results from multiple logistic regression models, after adjusting for age, sex, IADL and chronic conditions showed that participants under the T cutoff were associated with exhaustion and those below the S cutoff were associated with slow walking speed. The adjusted logistic models for age, sex, IADL and chronic conditions showed significant association between T and frailty (OR 2.81, 95% CI 1.29-6.12), but not between S and frailty (OR 1.73, 95% CI 0.83-3.63).
Conclusions
Taste and smell perception, particularly taste perception, were associated with a greater risk of frailty in community-dwelling elderly people. These results suggest that lower taste and smell perception may be an indicator of frailty in old age.
Key words: Frailty, taste, smell, elderly, AHSP
Abbreviations
- AHSP
Appetite, Hunger, Sensory Perception questionnaire
- T
total score of 8 Taste items
- S
total score of 6 Smell items
- BMI
Body Mass Index
- ROC
Receiver Operator Curves
- AUC
Area Under the Curves
- YI
Youden Index
Introduction
Frailty is a common geriatric syndrome that is defined as the status of increased vulnerability for adverse health outcomes, including falls, disability, hospitalization, and mortality (1). Without a consensus, frailty has been operationally defined as meeting three out of five of the following criteria: unintentional weight loss, self-reported exhaustion, weakness, slow walking speed and low activity (1, 2). Several studies have shown that aging, gender, skeletal muscle disuse and cognitive function are associated factors of frailty (1, 3, 4, 5). Further, loss of appetite and reduced food intake are also known related factors of frailty (6, 7).
Taste and smell perception is important for elderly health. Declines in taste and smell have been well documented in elderly people, which can lead to poor appetite and hunger (8), inappropriate food choices (9), and lower nutrient intake (10). Previous research has shown that flavor enhancement of foods increase food intake in elderly subjects with deficits in taste and smell (11).
However, there is still a lack of information about the association between taste and smell perception and frailty status, particularly the frailty criteria. The purpose of this study was to explore the relationship between frailty and taste and smell perception in community-dwelling elderly people.
Subjects and method
There were 108,111 people living in the Itabashi ward as of September 1, 2013, and 7,162 (6.6%) lived in the Southeastern area of the ward. To maintain a representation of this larger population, a letter inviting people older than 65 years to participate in a comprehensive geriatric health examination survey was sent to 6,699 community–dwelling people randomly selected from the Basic Resident Register of the Itabashi ward. There were 1,183 people who responded to the invitation, and among them, 791 elderly participated in the survey conducted at the Tokyo Metropolitan Institute of Gerontology (TMIG). A total of 768 participants without missing data were used for the analyses. This study protocol was approved by the Clinical Research Ethics Committee of TMIG. Procedures were fully explained to all participants, and written informed consent was obtained.
Data collection
Interview survey
Face-to-face interviews were conducted to assess taste and smell perception, instrumental activities of daily living (IADL), and chronic conditions. IADLs were assessed using the Instrumental Self-Maintenance dimension of the TMIG index (12) of competence. For each of 5 items (public transportation, shopping, food preparation, payment, handle finances), “yes” was scored as 1 and “no” as 0 (maximum score: 5). Chronic conditions were assessed by the history of the following diseases: hypertension, stroke, heart disease, diabetes, hyperlipidemia, osteoporosis, anemia, chronic renal failure, bronchial asthma and chronic obstructive pulmonary disease, “yes” was scored as 1 and “no” as 0 (maximum score: 10).
Taste and smell perception
Fourteen out of 29-items of the Appetite, Hunger, Sensory Perception questionnaire (AHSP) (13) were used to assess taste (8 items) and smell perception (6 items). The questions were answered on 5-point Likert scales with verbally labeled answering categories. Every answer was coded from 1 to 5. This tool was tested against taste perception test and a small identification test (8). Those items of the original article were translated from English to Japanese. The total score of 8 taste items (T, range 8-40) and 6 smell items (S, range 6-30) were used for analysis.
Anthropometric and Physical Function
Measurements of height and weight were converted to BMI. Grip strength was measured using a hand-held Smedley type dynamometer. Usual walking speed was measured on a flat, 11-m walking path, with markers at the 3-m and 8-m points, where participants were asked to walk the full 11m. A stopwatch was used to measure the time taken to walk 5m between the markers, and the faster of 2 trials was recorded.
Frailty
Frailty was diagnosed using a modified Fried's frailty phenotype criteria (1), 1) unintentional weight loss: having unintentionally lost more than 2.0~3.0kg in the last 6 months. 2) Self-reported exhaustion. Answering “yes” to the question “Have you feel tired with no reason in these two weeks?” 3) Weakness: hand grip strength less than 20 kg in women and 30 kg in men (14). 4) Slow walking speed: usual walking speed less than 1.0m/s (15). 5) Low activity: Answering “yes” to at least three of the following 4 statements, “I regularly take walks less than once a week,” “I regularly take light exercise less than once a week,” “I do not regularly take exercise and sports except for walking and light exercise,” and “I do not actively participate in hobbies or lessons of any sort.” The presence of three or more of the above mentioned five components were classified as frailty (FFigure 1).
Figure 1.
Detailed flow chart of participants
Data analysis
Data were presented as mean ± standard deviation (SD) for continuous variables and percentages for categorical variables. The internal consistency reliability of the taste and smell perception questionnaire was estimated using the Cronbach's alpha coefficient. The accuracy of each perception score (T, S) in assessing frailty was assessed by Receiver Operator Curves (ROC) and the area under the curves (AUC). Sensitivity, specificity and the Youden Index (YI) were analyzed to determine the optimal cutoff score to reflect frailty. To compare taste and smell perception above and below the cutoff values, the difference between continuous variables was assessed by non-paired t-test and distributions of categorical variables were compared using Chi-square tests.
Multiple logistic regressions were used to analyze the association between sensory perception and frailty criteria, weight loss, exhaustion, poor muscle strength, slow walking speed and poor physical activity, or frailty. Factors potentially associated with frailty were included in the model. Age and gender were forced into the models of the multiple logistic regression analyses to obtain the odds ratio (OR) and 95 % confidence intervals (CI).
P values less than .05 were considered statistically significant. All analyses were performed with SPSS software (version 20.0 of windows, IBM, Tokyo, Japan).
Results
The mean age (±SD) of the participants in the present study was 73.5 ± 5.6 (Table 1). Participants were predominantly women (56.9%) with normal BMI 22.9 ± 3.2 and 45 participants (5.9%) were defined as frail (Table 1).
Table 1.
Summary of subject characteristics
| Variable | M±SD* |
|---|---|
| Age (y) | 73.5±5.6 |
| Female (%) | 56.9 |
| IADL | 4.9±0.5 |
| Chronic conditions | 1.4±1.2 |
| BMI (kg/m2) | 22.9±3.2 |
| Frailty criteria | |
| Weight loss (%) | 13.5 |
| Weakness (%) | 21.1 |
| Slow walking speed (%) | 6.4 |
| Exhaustion (%) | 16.0 |
| Low activity (%) | 21.9 |
All values are means ± SD for continuous variables and percentages for categorical variables.
The reliability analysis indicated by Cronbach's alpha coefficient of T was 0.695 and S was 0717. Analyzing receiver operator curves for detection of frailty, the area under the curve (AUC), demonstrated that T (0.715, 95% CI: 0.635 - 0.795) had moderate accuracy, but S (0.657, 95% CI: 0.578 - 0.736) had low accuracy (Figure 2).
Figure 2.
Receiver operator curves for the Taste and Smell Perception score using frailty as the reference. (A) Taste 8 items score, area under the curve (AUC) = 0.715 (95% CI: 0.636-0.795), Cutoff score was 26.5 (Youden Index (YI) = 0.350, sensitivity: 0.639, specificity: 0.711). (B) Smell 6 items score, AUC = 0.657 (95% CI: 0.578-0.736), Cutoff score was 18.5 (Youden Index (YI) = 0.246, sensitivity: 0.690, specificity: 0.556)
Compared to subjects over the T cutoff, those under the cutoff were older (mean age: 74.3 vs 73.0), more functionally impaired (mean IADL: 4.8 vs 4.9), had greater chronic conditions (mean number of chronic condition: 1.5 vs 1.3) and were frail (10.9 vs 2.7 %); i.e. have weaker hand grip strength (27.3 vs 17.3 %), slower walking speed (9.9 vs 4.2 %), more exhaustion (24.6 vs 10.7) and lower activity (26.6 vs 18.9%) (Table 2). Similarly, compared to subjects over the S cutoff, those below the cutoff were older (mean age: 74.9 vs 72.9), and more likely to be frail (10.0 vs 3.9 %); weaker hand grip strength (26.5 vs 18.5 %), slower walking speed (11.2 vs 4.0 %), more exhaustion (20.9 vs 13.7) and lower activity (27.7 vs 19.1%, Table 3).
Table 2.
Comparison of selected variables and frailty between subjects above and below the taste perception cutoff value (using 8 taste items)
| Variable |
Taste_8 <26.5 (n=293) |
Taste_8 >26.5 (n=475) |
P-value |
|---|---|---|---|
| Age (y) | 74.3±5.4 | 73.0±5.7 | 0.002 |
| Female (%) | 53.6 | 58.9 | 0.154 |
| IADL (score) | 4.8±0.7 | 4.9±0.3 | 0.003 |
| Chronic conditions (points) | 1.5±1.2 | 1.3±1.2 | 0.004 |
| BMI (kg/m2) | 22.8±2.9 | 23.0±3.3 | 0.552 |
| Frailty criteria | |||
| Weight loss (%) | 15.7 | 12.2 | 0.193 |
| Weakness (%) | 27.3 | 17.3 | 0.001 |
| Slow walking speed (%) | 9.9 | 4.2 | 0.002 |
| Exhaustion (%) | 24.6 | 10.7 | <0.001 |
| Low activity (%) | 26.6 | 18.9 | 0.015 |
| Frailty (%) |
10.9 |
2.7 |
<0.001 |
Data presented as mean ± SD for continuous variables and percentages for categorical variables.
Table 3.
Comparison of selected variables and frailty between subjects above and below the smell perception cutoff value (using 6 smell items)
| Variable | Smell_6 <18.5 (n=249) | Smell_6 >18.5 (n=519) | P-value |
|---|---|---|---|
| Age (y) | 74.9±5.4 | 72.9±5.6 | <0.001 |
| Female (%) | 51.8 | 59.3 | 0.052 |
| IADL (score) | 4.9±0.6 | 4.9±0.4 | 0.091 |
| Chronic conditions (points) | 1.4±1.2 | 1.3±1.2 | 0.157 |
| BMI (kg/m2) | 22.9±3.1 | 22.9±3.3 | 0.856 |
| Frailty criteria | |||
| Weight loss (%) | 14.5 | 13.1 | 0.652 |
| Weakness (%) | 26.5 | 18.5 | 0.014 |
| Slow walking speed (%) | 11.2 | 4.0 | <0.001 |
| Exhaustion (%) | 20.9 | 13.7 | 0.015 |
| Low activity (%) | 27.7 | 19.1 | 0.009 |
| Frailty (%) |
10.0 |
3.9 |
0.001 |
Data presented as mean ± SD for continuous variables and percentages for categorical variables.
After adjusting for age, sex, IADL and chronic conditions, the analysis into the association between taste/smell perception and the frailty criteria revealed that taste impairment (below the T cutoff) was significantly associated exhaustion (OR 2.36, 95% CI 1.52-3.67); and smell impairment (below the S cutoff) was significantly associated with slow walking speed (OR 2.46, 95% CI 1.21-5.03) (Table 4).
Table 4.
Association between taste and smell perception, and individual frailty criteria
| Weight loss | Weakness | Slow walking speed | Exhaustion | Low activity | |
|---|---|---|---|---|---|
| Variable | Odds ratios [95% Confidence interval] | ||||
| Taste_8 | 1.21[0.76-1.93] | 1.37[0.91-2.07] | 1.32[0.65-2.67] | 2.36[1.52-3.67]** | 1.29[0.88-1.90] |
| Smell_6 | 0.94[0.58-1.53] | 1.12[0.73-1.70] | 2.46[1.21-5.03]* | 1.09[0.70-1.71] | 1.44[0.97-2.13] |
| Age | 1.02[0.98-1.06] | 1.11[1.07-1.15]** | 1.11[1.04-1.18]** | 1.05[1.01-1.09]* | 1.00[0.97-1.03] |
| Gender | 0.83[0.54-1.26] | 1.04[0.71-1.51] | 1.49[0.76-2.94] | 1.88[1.22-2.88]** | 1.05[0.74-1.50] |
| IADL | 0.83[0.58-1.19] | 0.38[0.24-0.61]** | 0.23[0.14-0.39]** | 0.59[0.41-0.85]** | 0.67[0.48-0.93]* |
| Chronic conditions |
1.30[1.10-1.53]** |
1.22[1.05-1.42]** |
1.21[0.94-1.57] |
1.17[0.99-1.38] |
0.97[0.84-1.12] |
Dependent variable of interest is frailty criteria, weight loss, exhaustion, weakness, slow walking speed and low activity. Taste_8, smell_6 were analyzed for ≤ cutoff as 1, ≥ cutoff as 0
<0.05
<0.01
Finally, the adjusted logistic models for age, sex, IADL and chronic conditions showed significant association between T and frailty (OR 2.81, 95% CI 1.29-6.12), but not between S and frailty (OR 1.73, 95% CI 0.83-3.63; Table 5).
Table 5.
Adjusted odds ratios (OR) and 95% confidence intervals (CI) of taste and smell for frailty
| Independent Variable | OR | 95 CI | P-value |
|---|---|---|---|
| Taste_8 | 2.81 | 1.29-6.12 | 0.01 |
| Smell_6 | 1.73 | 0.83-3.63 | 0.15 |
| Age | 1.11 | 1.04-1.18 | <0.001 |
| Gender | 0.84 | 0.42-1.68 | 0.62 |
| IADL | 0.24 | 0.14-0.40 | <0.001 |
| Chronic conditions |
1.44 |
1.10-1.88 |
0.01 |
Dependent variable of interest is frailty. Taste_8, smell_6 were analyzed for ≤ cutoff as 1, ≥ cutoff as 0.
Discussion
To our knowledge, this is the first study investigating the association of frailty and taste and smell perception in community-dwelling elderly people. The results suggest that decline in taste and smell perception are associated with a greater risk of frailty in elderly people. After adjusting for age, sex, IADL and chronic conditions, taste was associated with exhaustion within the frailty criteria, while smell was associated with slow walking speed. Interestingly, taste was more strongly associated with frailty.
In this study, the translated questionnaire of taste and smell perception in the AHSP was used (13). Smell perception in the AHSP has been demonstrated to be associated with the smell identification test (8, 16). Whereas previous research has found that the 29 item AHSP questionnaire was difficult to answer by the hospitalized patients in a geriatric rehabilitation care because of the high prevalence of cognitive impairment (17), the 14 item taste and smell perception questionnaire has been able to be answered by community-dwelling elderly people in this study. The internal validity of our study by Cronbach's alpha coefficient was moderate.
The rate of frailty, as determined by Fried's criteria was 5.9%. This rate was within the previously reported Japanese prevalence of frailty also using Fried's ctiteria, 2.7 % (18) and 11.3 % (19). Other studies using different definitions of frailty reported a prevalence of frailty 10.0 %(20), 16.0 % (21) and 22.8 %(22).
The results of this study revealed that sensory perception was associated with weak hand grip strength, slow walking speed, exhaustion and low activity, but not body weight loss or BMI. Although some studies have shown that taste and smell perception scores were different between various health groups i.e., independently living elderly vs institutionalized elderly (8) and free-living without help, free-living with help and nursing home (13); as far as we know this is the first study to report the link between sensory perception and frailty using validated screening tools for these conditions. On the other hand, regarding body weight, the results were inconsistent with those of De Jong's report (8), that taste and smell perception was related to body weight in Dutch elderly people. Ethnic difference between the subjects may be a possible explanation. Further research on Japanese populations is necessary.
Declines in taste and smell perception may be associated with risk of frailty in elderly people. One possible mechanism is that reduction of taste and smell decrease appetite and food intake, which has been reported to be associated with frailty (6, 7). However in this study, no significant associations were seen between smell and taste perception and body weight loss. Regardless, taste perception was associated with exhaustion and smell perception with slow walking speed. Based on the frailty cycle by Xue et al, undernutrition caused by reduced sense of smell and/or taste may negatively affect body composition, muscle mass in particular (23). The exhaustion and the reduction in walking speed may lead to sarcopenia, and in turn, frailty.
Self-reported taste perception is more strongly associated with frailty than smell perception. One possible explanation may be that people often misinterpret a loss or change in food flavors as a problem with their sense of taste not smell (24) and self-reported olfactory impairment underestimated prevalence rates obtained by odor identification test in elderly (25). The other, eight items of taste include broad question; enjoyment of food, not only the sensation produced by basic tastes, such as sweetness, saltiness, bitterness, sourness and umami, while smell question does not include those broad question about food.
The results of the present study suggest that the taste portion of AHSP, with cutoff score 26.5, can be used to identify community-dwelling elderly people at risk of frailty. More detailed testing, such as complete geriatric assessment, Fried scale and objective taste and smell tests, can then be undertaken on those with decreased taste perception so that individual nutritional management programs can be implemented.
Some of the limitations of this study should be discussed. The cross-sectional design of this study does not permit to clarify any cause–effect mechanism. Furthermore, we were unable to compare the 768 (11.5%) of participants included in the study with non-participants; therefore, the results should be interpreted with consideration of potential selection bias. Another weakness is that there is no data of cognitive score, depression, smoking and limited adjustment. Finally, our results may not be generalizable to other countries because of difference in the socio-economic system in various countries.
In conclusion, taste and smell perception, in particular taste perception, associate with the greater risk of frailty in community-dwelling elderly. These results suggest that lower taste and smell perception may be an indicator of frailty in old age.
Acknowledgement: We thank E. Hosoi, who assisted in the revision of the manuscript. We acknowledged Dr. N. Sakai, Tohoku University, for the translation of the AHSP.
Conflict of Interest: This study was supported by a Grant-in-Aid for Scientific Research B from the Japanese Society for the Promotion of Science (26282201). The authors have no conflict of interest to disclose.
Author Contributions: The author's responsibilities were as follows – SO, HY, YF, HH, KI and HKim designed the research; TM, KO, NH, SO, HY, HKawai, YF, HH, MK, KI and HKim conducted the research; SS and HKim performed statistical analyses; SS and HKim wrote the paper; HKim holds primary responsibility for final content of the manuscript.
Funding Identified: This study was supported by a Grant-in-Aid for Scientific Research B from the Japanese Society for the Promotion of Science (26282201)
Ethical Standards: Experiments comply with the current laws of the country in which they were performed.
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