Journal of Clinical Nutrition & Dietetics

Keywords

Frailty; Dietary intake; Physical activity; Nutritional status

Introduction

Frailty is a geriatric syndrome characterized by a diminished capacity of the organism to respond to external stressors and an increased vulnerability to suffer falls, functional decline, incapacity, dependency, institutionalization and even death [1]. Its prevalence increases with age and can reach 50% in adults 80 years or older [2], representing a serious public health problem that needs to be urgently addressed [3]. The pathophysiology of frailty is not well established. Rockwood et al. [4] considered that frailty results from the accumulation of unrelated diseases, dysfunctions and disabilities, but Fried et al. [5] considered frailty to be a unique pathophysiological process involving the breakdown of homeostatic mechanisms. Fried proposed a definition of the frailty phenotype in which muscle wasting was the major component. Different factors have been related to loss of muscle mass and function such as inflammatory processes, anabolic hormone declines, physical inactivity or under nutrition [6]. There is evidence suggesting that exercise and caloric and protein support may have a positive effect on frailty [7-9]. However, few studies on community-dwelling older people have directly related dietary habits, energy and protein intake and energy expenditure with frailty and pre-frailty status. The aim of this study was to describe dietary habits in a community-dwelling older population and to assess whether dietary energy intake and energy expenditure by physical activity was related to frailty and pre-frailty status.

Methodology

Study design and population

An observational, population-based, cross-sectional study was performed on community-dwelling adults aged 75 years and older. A sample was randomly selected from the database of 3 primary care centres in the municipalities of Mataró and Argentona (Barcelona, Spain) on the western Mediterranean coast. Individuals were excluded if they had active malignancy, dementia or serious mental illness, had a life expectancy of less than 6 months, were in a palliative care programme or were institutionalized. Swallowing disorders were not exclusion criteria. Person who fulfilled all selection criteria and who signed the informed consent form were recruited from January to July 2014. A total of 324 persons were recruited, 170 men and 154 women, with a mean age of 80.1 years (min. 75, max.93).

Definition of frail

People were classified as robust, pre-frail or frail according to the Fried criteria [5]. The following five criteria were assessed: a) Unintentional weight loss of ≥ 4.5 kg in the last 12 months, b) Exhaustion, defined by a response of 3 days or more to either or both of 2 questions: “How often in the last week did you feel you could not get going?” and “How often in the last week did you feel that everything you did was an effort? c) Low physical activity, defined as total weekly kcal of physical activity expenditure < 383 kcal in men or < 270 kcal in women, d) Slow walking speed, defined as < 0.65 m/s for a height of ≤ 173 cm in men / ≤ 159 cm in women or < 0.76 m/s for a height of > 173 cm in men / > 159 cm in women, e) Poor grip strength (using a handheld JAMAR dynamometer), defined as ≤ 29 kg for body mass index (BMI) ≤ 24, ≤ 30 kg for BMI 24.1 - 28 and ≤ 32 kg for BMI > 28 in men or ≤ 17 kg for BMI ≤ 23, ≤ 17.3 kg for BMI 23.1-26, ≤ 18 kg for BMI 26.1 - 29 and ≤ 21 kg for BMI > 29 in women. Persons were classified as robust if they fulfilled none of the above criteria; pre-frail if they fulfilled 1 or 2 criteria; and frail if they fulfilled 3 or more criteria.

Study factors and data collection

Dietary intake was assessed by a food frequency consumption questionnaire validated in Spain [10] which registers the frequency individuals eat 45 different foods over a week. Each serving of food was converted into grams of carbohydrates, lipids, proteins and fiber intake according to the BEDCA database of food composition (https://www.bedca.net/). Finally, grams of ingested carbohydrates, lipids and proteins were converted into Kcal intake. In addition, grams of ingested fiber and alcohol intake were also estimated from the same questionnaire. Nutritional status was assessed by anthropometric measurements (weight, height, BMI) and the short-form of the Mini Nutritional Assessment (MNA-sf) which classifies individuals as well nourished (12 - 14 points) or at risk of malnutrition (< 12 points) [11]. Physical activity was assessed by the International Physical Activity Questionnaire (IPAC) [12]. This questionnaire estimates total METs (metabolic equivalent of task) for severe, moderate or mild physical activity and for overall physical activity. To convert 1 MET into kcal/min the following equation applies: Kcal/min = 0.0175 × MET × weight (kg). Other study variables included socio-demographic characteristics, co-morbidities and chronic medication. Information on comorbidities and medication was obtained from the electronic medical records held by each centre. All other information was obtained directly from the patient by healthcare professionals.

Ethics

No person was recruited without signing the informed consent form. The research ethics committee from Consorci Sanitari del Maresme approved the study protocol and documentation (code 64 / 13).

Statistical analysis

Continuous variables were described using means and standard deviations and categorical ones using percentages. Comparisons across the 3 study groups (robust, pre-frail and frail) were made using ANOVA or the Kruskal-Wallis test for numerical variables and the X² test or the Fisher’s exact test for categorical ones. To evaluate factors associated with frailty, the robust and prefrail groups were pooled together in a non-frail group and frail versus non-frail persons were compared. Comparisons between 2 groups (non-frail and frail) were made using the t-test or Mann-Whitney U test for numerical variables and the X² test or the Fisher’s exact test for categorical ones. The effect (OR) of the variables associated with frailty was estimated by logistic regression analysis. Statistical significance was established at p < 0.05.

Results

A sample of 324 persons was recruited (52.5% men and 47.5% women) with a mean age of 80 (3.5) years. Main co-morbidities were arterial hypertension (70.0%), osteoarthritis (52.4%), dyslipidaemia (50.9%), diabetes (24.2%), ischemic heart disease (21.5%) and depression (19.6%). Participants were taking a mean of 6 medications. Gender was related to frailty, as women represented 28.8% of the robust group, 51.1% of the pre-frail group and 76.1% of the frail group (p < 0.001).

Table 1 shows the dietary intake of the whole sample and for robust, pre-frail and frail groups. It shows that participants ate more than 15 servings of fruit a week and more than 12 servings of vegetables a week. Frail older persons ate more soups and white fish but fewer non-citric fruits, dried fruits (like nuts), and salads, and drank less wine and beer than non-frail. When all fruit servings (citric fruits, non-citric fruits and nuts) were pooled together we observed that eating ≤ 2 fruit servings / day was a risk factor for frailty with an OR = 1.90 (95% CI: 1.01 - 3.56, p = 0.046). Similarly, when all vegetables servings were pooled we observed that eating ≤ 1 vegetable servings / day was a risk factor for frailty with an OR = 1.93 (95% CI: 1.03 - 3.62, p = 0.041). Moreover, a fibre intake ≤ 23 g/day was a risk factor for frailty with an OR=2.86 (95%CI: 1.49 - 5.50, p = 0.002). Frail men eat less shellfish and nuts and drink more low-calorie beverages, while frail women eat less bread, ham and non-citric fruits and eat more yogurts, soups, and cakes. According to MNA-sf, 5.4% of the whole sample was classified as “at risk of malnutrition”, with significant differences between groups (2.0% in robust, 4.7% in pre-frail, and 15.6% in frail; p = 0.003). BMI was in the overweight range in men, with no significant differences between groups (29, 28, and 27 for frail, pre-frail and robust, respectively). BMI was significantly higher in frail and pre-frail women in comparison to robust women (30, 30, and 26, respectively; p < 0.001). Nutritional status was not related with dietary intake of the various foods considered except for salads, green beans and eggs, which were more frequent in well nourished.

Table 1: Dietary habits by frailty groups in community-dwelling older people.

Table 2 compares total energy intake, lipid, protein and carbohydrate calorie intake, total fibre and alcohol intake as well as energy expenditure through physical exercise, total energy expenditure (metabolic rate + expenditure through physical exercise) and energy balance (total energy intake - total energy expenditure) between groups. It shows that frail persons had lower overall calorie intake, lower fibre and alcohol intake, as well as lower calorie expenditure and higher positive energy balance. Calorie expenditure through physical exercise ≤ 100 Kcal/day was a risk factor for frailty with an OR = 14.4 (95% CI: 7.06 - 29.5, p < 0.001).

Table 2: Macronutrient intake, calorie intake and calorie expenditure by frailty groups.

Discussion

The results of the present study show that: a) a communitydwelling older population in a town on the west coast of the Mediterranean Sea tended to have a diet rich in nuts, fruits and vegetables, b) they had a good nutritional status, c) there were no major differences in protein intake between frail and nonfrail persons, d) frail persons had a lower intake of salads, nuts, fruits and fibre, and e) frail persons had lower calorie intake and a much lower calorie expenditure than non-frail persons with a greater positive energy balance.

Nutrition is thought to play a major role in the development of frailty. Weight loss is one of the defining criteria of frailty [5] and large observational studies have suggested that poor nutritional status promotes frailty [13]. Weight loss is highly indicative of frailty (it has a high specificity), although relatively few frail persons have this frailty criteria (it has a low sensitivity) [14] indicating that other risk factors such as low physical activity, co-morbidities or chronic inflammation are also of critical relevance in the genesis of frailty. Frail persons have lower energy, macronutrient and micronutrient intake than nonfrail persons [15]. The results of the present study agree with the existing evidence in showing a lower calorie intake in frail persons. However, we observed no differences between frailty groups in macronutrient intake (mainly protein and fat intake) although frail persons clearly ate less fruit, nuts, vegetables and fibre. Fruits and vegetables are important components of the Mediterranean diet and have been identified as a relevant part of the diet in preventing age-related diseases [16, 17]. There is growing evidence that adherence to the Mediterranean diet protects individuals against cardiovascular diseases and other chronic diseases, some cancers [18, 19], mobility decline, low walking speed and low physical activity, suggesting a relationship between diet and frailty [20, 21]. Although the majority of studies on the health benefits of fruits and vegetables do not include older populations, there is growing evidence that fruit and vegetable intake in older adulthood can prevent cognitive impairments and dementia, heart diseases, functional decline and walking speed [22, 23]. A recent publication by Chan et al. showed that higher vegetable and fruit intake was associated with a lower prevalence of sarcopenia in older Chinese men [24]. Moreover, higher serum carotenoid levels are associated with improved muscle strength and bone density in older people [25-27], suggesting that fresh fruit and vegetable intake, the main source of vitamins, carotenoids and micronutrients with antioxidative capacity, can protect against physical function decline, frailty and disability. On the other hand, protein intake has been inversely related to loss of lean mass in community-dwelling older people in the Health, Ageing, and Body Composition Study (ABC Study) [7] and high protein intake showed a 32% reduction in the risk of frailty in postmenopausal women in the Women’s Health Initiative [28]. However, the role of protein supplementation in reducing the risk of sarcopenia and frailty is controversial since a systematic review including 62 randomized clinical trials (with 10,187 participants) showed little evidence on the benefit of this intervention in improving functionality and showed no significant effect on reduction of mortality, except for undernourished persons [29, 30]. In the present study we did not find differences in protein intake between study groups. These results may be explained by the fact that all study groups showed good protein intake according to the international recommendations for older people (1 g -1.5 g of proteins/Kg/day). The ABC Study established a link between protein intake and loss of lean body mass when protein intake was insufficient or low (0.7 g of proteins/kg/day) in comparison to high protein intake (1.1 g of proteins/kg/day). In our study, protein intake was in the high protective range in all groups.

Regarding exercise, the present study showed a reduction in physical activity as the frailty process developed, with a significant reduction of total calorie expenditure in pre-frail with respect to robust persons and frail with respect to pre-frail persons. The reduction in total calorie expenditure in frail persons was much greater than the reduction in total calorie intake. These results indicate a positive energy balance in frail persons, leading to a sarcopenic obesity pattern. These results agree with most scientific evidence on the effect of physical activity on muscle strength in older persons. A review of the Cochrane Collaboration that summarized 49 clinical trials concluded that there was good evidence for the effectiveness of exercise programs in older people [8] and another meta-analysis including 8 clinical trials showed that exercise was able to improve walking speed, balance and functional capacity in frail older people [9]. Physical inactivity and loss of muscle strength form a vicious circle difficult to break. Poor muscle strength is the most prevalent frailty component and has been related to physical activity [14]. Changing habits and motivating older people to practice regular physical exercise is a necessary and major challenge for health professionals to prevent frailty and functional decline.

The present study has three main limitations, a) the cross-sectional design does not allow causal relationships to be established, but only associations between variables, because of the temporal ambiguity between frailty and studied risk factors, b) the relatively small sample size which limits the statistical power for small effects and low-prevalence risk factors and c) Indicators of total calorie intake and total calorie expenditure were estimated by validated questionnaires, which provide estimations with known limited accuracy. This possible misclassification is the same for all three study groups, so it can reduce the expected effect but not introduce any bias.

Conclusion

In conclusion, nutrition and physical activity are probably the greatest modifiable predictors of heath in old age. The present study showed that in an older population with sufficient calorie and protein intake in a largely Mediterranean diet, lower micronutrient intake of nuts, fruits and vegetables was a risk factor for frailty. Moreover, lower calorie expenditure through physical activity was also related to frailty and to predispose to a positive energy balance and a sarcopenic obesity pattern. Health care practitioners must encourage and motivate older people to exercise regularly and maintain good dietary habits including both good calorie and protein intake and good micronutrient (mainly vitamins, antioxidants and trace elements) intake.

Acknowledgement

This study was funded by grants from the Spanish Ministry of Health: Instituto de Salud Carlos III, Fondo de Investigación Sanitaria (PI 13 / 00931).

Conflict of Interest

The authors declare that they have no conflict of interest.

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