Dietary Protein Intake Is Protective Against Loss of Grip Strength Among Older Adults in the Framingham Offspring Cohort

Abstract

Background:

Age-related decline in muscle strength is an important public health issue for older adults. Dietary protein has been associated with maintenance of muscle mass, yet its relation to muscle strength remains unclear.

Methods:

We determined the association of dietary protein (total, animal, and plant) intake, measured by food frequency questionnaire, with change in grip strength over 6 years in 1,746 men and women from the Framingham Offspring cohort.

Results:

Mean age at baseline was 58.7 years (range: 29–85), and mean total, animal, and plant protein intakes were 79, 57, and 22g/d, respectively. Adjusted baseline mean grip strength did not differ across quartiles of energy-adjusted total, animal or protein intake. Greater protein intake, regardless of source, was associated with less decrease in grip strength (all p for trend ≤.05): participants in the lowest quartiles lost 0.17% to 0.27% per year while those in the highest quartiles gained 0.52% to 0.60% per year. In analyses stratified by age, participants aged 60 years or older ( n = 646) had similar linear trends on loss of grip strength for total and animal (all p for trend <.03) but not plant protein, while the trends in participants younger than 60 years ( n = 896) were not statistically significant.

Conclusions:

Higher dietary intakes of total and animal protein were protective against loss of grip strength in community-dwelling adults aged 60 years and older. Increasing intake of protein from these sources may help maintain muscle strength and support prevention of mobility impairment in older adults.

With the population of older adults rapidly growing and living longer, the public health burden of physical disability is expected to dramatically increase in the coming decades ( 1 ). Age-related decline in muscle strength is a major contributor to impaired function and disability ( 2 ), thus understanding the determinants of loss of muscle strength is essential to develop novel interventions that effectively maintain muscle health.

Change in diet with aging has become increasingly recognized as a potentially modifiable lifestyle determinant of muscle strength ( 3 ). Dietary protein intake has been the focus of several epidemiologic investigations ( 3–9 ) as the amino acids it provides are necessary for muscle protein synthesis ( 10 ). Results from cross-sectional observational studies of dietary protein and handgrip strength are conflicting ( 3–5 ), and there has been only one longitudinal study suggesting that women with higher protein intake have slower declines in grip strength ( 6 ). Thus, the impact of dietary protein intake on age-related loss of muscle strength in population-based cohorts remains unclear. Furthermore, while previous studies provide some evidence that greater dietary protein may help slow the age-related loss of lean mass ( 11 , 12 ), none have evaluated whether the influence of protein on muscle strength involves a pathway through lean muscle mass.

We determined the association of dietary protein intake with baseline and longitudinal change in grip strength among men and women from the Framingham Offspring cohort. We hypothesized that higher protein intake (total, animal, and plant) would be associated with higher grip strength at baseline and lower loss of grip strength, and that arm lean mass would, at least partially, explain these associations.

Methods

Study Population

Study participants included members of the Framingham Offspring cohort. From 1971 to 1975, 5,124 men and women were enrolled (age range 5–70 years at enrollment) and subsequently examined at approximately 4-year intervals to investigate familial risk factors for cardiovascular disease among the adult children, and their spouses, of the population-based Framingham Original Cohort ( 13 ). The current study includes the 1,746 participants who had a valid dietary assessment completed in either 1995–1998 or 1998–2001, grip strength measured in 1999–2002, and lean mass measured in 1996–2001 (baseline). Of these, 1,542 had a follow-up grip strength assessment in 2005–2008 and were thus eligible for inclusion in longitudinal analyses. This study was approved by the institutional review boards at Hebrew SeniorLife and Boston University and informed consent was obtained from all participants.

Dietary Protein Intake

At baseline, usual dietary intake was assessed with the semiquantitative, 126-item Willett food frequency questionnaire (FFQ) ( 14 ). The FFQ was mailed to study participants who were asked to complete the questionnaire based on their food intake over the previous year, and to bring it to the exam site where it was reviewed by clinic staff. Questionnaires with more than 12 food items left blank, or energy intakes <600 or >4,000 kcal, were considered invalid and excluded. The Willett FFQ has been validated for several nutrients, including protein, against diet records, and blood measures in various populations ( 15 ). Intake of total protein (g/d), and of protein specifically from animal and plant sources, was calculated using the food list section.

Grip Strength

At both baseline and follow-up, grip strength (kg) was measured using an adjustable Jamar isometric hand-held dynamometer. Participants were asked to maximally squeeze the dynamometer for 3 seconds. Three trials were attempted on each hand for a total of up to six trials, and the maximum value among all trials, regardless of side (left vs right), was used for the current study ( 16 ). Annual percent change in grip strength was calculated as ([grip strength at follow-up grip strength at baseline]/grip strength at baseline) × 100, divided by follow-up time in years.

Arm Lean Mass

At the time of baseline grip strength assessment, whole-body dual-energy X-ray absorptiometry scans were obtained using a Lunar DPX-L (LunarCorp, Madison, WI) as previously described ( 16 ). Arm lean mass (kg) was estimated as the lean mass of the arms region, which included both the right and left arms.

Other Variables

Covariate information was obtained from measures collected closest to the time of the X-ray absorptiometry exam and included sex, age, height, total energy intake, body mass index, physical activity, health status, and menopause status. Height without shoes (inches) was measured to the nearest quarter inch with a stadiometer. Weight, in light clothing, (pounds) was measured with a standardized balance-beam scale. Body mass index was calculated as weight in kilograms divided by the square of height in meters (kg/m ² ). Physical activity level was assessed as the Physical Activity Scale for the Elderly score, a validated questionnaire of self-reported activity over the past seven days ( 17 ). Total energy intake (kcal/d) was calculated from the FFQ. Self-reported health status was assessed by asking participants “In general, how is your health now?” and given the choice to respond excellent, good, fair, or poor. Percent fat of the arms region was ascertained from the X-ray absorptiometry scans. Participants were categorized into two menopause status groups: postmenopausal women (women who reported no menstrual periods for at least 1 year or current use of hormone replacement therapy) versus premenopausal women and men combined.

Statistical Analyses

Protein intake (total, animal, and plant) was modeled as both a continuous variable and categorized into quartiles. To determine the associations of each protein measure with grip strength (both baseline and change), multivariable linear regression was used to calculate regression coefficients (β) estimating the difference in baseline grip strength, and longitudinal change in grip strength, associated with a 1g/d increase in baseline protein intake. Analysis of covariance was used to compare least squares-adjusted baseline grip strength and grip strength change among quartiles of protein intake, using Tukey’s adjustment for all pair-wise multiple comparisons, and to test for linear trend across quartiles. For the quartile analyses, the residual method was used to adjust for energy intake ( 18 ). All analyses were also repeated with protein intake expressed as the percent of total energy intake. Results were similar, thus only results for protein expressed as g/d and adjusted using the residual method are presented.

All models were adjusted for sex, age, height, total energy, body mass index, physical activity, health status, and menopause status. To account for possible effects of an overall healthier diet, models were subsequently adjusted for fruit and vegetable intake (servings/d), from which plant sources of protein were excluded (correlation between fruit and vegetable intake and plant protein intake = 0.48, p < .01). Animal and plant protein intakes were adjusted for each other in the same model. To test for potential interaction by sex, we repeated all models including a sex × protein interaction term. There were no statistically significant sex interactions ( p range: .26 to .89), thus the results of analyses with sexes combined are presented.

For analyses of change in grip strength, models were adjusted for baseline grip strength. Additionally, to determine whether baseline arm lean mass may, at least partially, account for any association between dietary protein intake and change in grip strength, we first used multivariable linear regression (same model as above with the addition of percent arm fat) to determine whether protein intake (continuous) was associated with arm lean mass at baseline. If there was evidence of an association, baseline arm lean mass was then added to the regression models for baseline protein predicting change in grip strength. If the regression coefficient for protein was reduced by 10% or more after the addition of arm lean mass, then we considered that arm mass may partially mediate the association between protein and grip strength ( 19 ).

We observed an overall mean increase in grip strength between baseline and follow-up in our study population, which is likely due to the inclusion of younger adults who have not yet reached peak muscle strength ( 20 ). Thus, to evaluate the influence of protein intake on age-related muscle loss in older versus younger adults, we repeated our analyses of grip strength change stratifying the study population at age 60.

A nominal two-sided p value of .05 was considered statistically significant for all analyses. All analyses were conducted using SAS/STAT software version 9.3 (SAS Institute Inc., Cary, NC).

Results

Mean age in the study population at baseline was 59 years (range: 29–85) and 43.5% were men ( Table 1 ). Mean baseline grip strength was 32.4kg and the average total protein intake of 79g/d (1.0 gram of protein per kg body weight per day, g/kg/d) was higher than recommended levels (0.8g/kg/d), with the majority of intake from animal protein. Time between baseline and follow-up grip strength assessments ( n = 1,542) ranged from 1 to 8 years, with an average of 5.8 years, and the mean annual % change was 0.04%. Compared to the total study sample with baseline grip strength, participants who did not have a follow-up grip strength ( n = 204) had a higher proportion of men (53%), were older (mean age 65 years), but had similar grip strength (30kg) and total protein intake (79g/d) at baseline.

Table 1.

Baseline Characteristics of Participants From the Framingham Offspring Study ( n = 1,746) Presented as Means ± SD or %

Characteristics	Mean ± SD or %
Men (%)	43.5
Age (y) (range)	58.7±9.2 (29–85)
Height (inches)	65.9±3.6
Body mass index (kg/m 2 )	27.6±4.8
Physical activity for the elderly score	146.2±79.2
Follow-up time (y) (range)	5.8±1.0 (1–8)
Total energy intake (kcal/d)	1,846±595
Total protein (g/d)	79±27
Animal protein (g/d)	57±22
Plant protein (g/d)	22±9
Lean mass of the arms (kg)	5.4±1.8
Grip strength baseline (kg)	32.4±12.7
Grip strength change (%/y, n = 1,542)	0.04±6.2
Postmenopausal women (%)	20.0
Health status (%)
Excellent	41.5
Good	51.0
Fair	6.1
Poor	0.4

Dietary Protein and Baseline Grip Strength

While plant protein intake was inversely associated with baseline grip strength (β = −0.071±0.035, p = .04), there were no associations with either total (β < 0.0001±0.012, p = .99) or animal (β = 0.002±0.012, p = .88) protein. After adjustment for fruit and vegetable intake, the association between plant protein and baseline grip strength was attenuated and no longer statistically significant (β = −0.05±0.038, p = .16). In quartile analyses, there were no statistically significant trends in grip strength, and pair-wise comparisons revealed no significant differences ( Table 2 ).

Table 2.

Least Squares-Adjusted* Mean Baseline Handgrip Strength (± SE ) for Quartiles of Dietary Protein Intake (g/d) in 1,746 Men and Women From the Framingham Offspring Cohort

Protein Source	Quartile	Median Protein Intake (g/d)	Grip Strength (kg)	p for Trend
Total	1	63	32.6±0.37	.83
	2	74	32.2±0.36
	3	82	32.4±0.37
	4	94	32.5±0.37
Animal †	1	41	32.7±0.38	.93
	2	51	32.1±0.36
	3	60	32.3±0.36
	4	74	32.5±0.37
Plant †	1	16	32.7±0.38	.06
	2	20	32.6±0.36
	3	23	32.7±0.36
	4	27	31.6±0.37

*Adjusted for sex, age, height, total energy (residual method), body mass index, physical activity, health status, and menopause status.

^† Animal and plant protein intakes adjusted for each other as a continuous, energy-adjusted variable.

Dietary Protein and Grip Strength Change

There were positive associations of total (β = 0.021±0.01, p = .02), animal (β = 0.020±0.01, p = .03), and plant (β = 0.074±0.03, p = .01) protein intakes with annualized percent change in grip strength. In quartile analyses, participants in the lowest dietary protein quartiles lost 0.17% to 0.27% per year while those in the highest quartiles gained 0.52% to 0.60% per year, and trends across quartiles were statistically significant (all p ≤ .05) ( Table 3 ). There were, however, no differences among quartiles for any of the different sources of protein. Results were similar after adjustment for fruit and vegetable intake (data not shown).

Table 3.

Least Squares-Adjusted* Mean Percent Change in Grip Strength ( SE ) for Quartiles of Dietary Protein Intake (g/d) in 1,542 Men and Women From the Framingham Offspring Cohort

Protein Source	Quartile	Median Protein Intake (g/d)	Change in Grip Strength (%/year)	p for Trend
Total	1	63	−0.27 (0.29)	.05
	2	74	−0.15 (0.29)
	3	82	0.07 (0.28)
	4	95	0.52 (0.29)
Animal †	1	41	−0.17 (0.30)	.03
	2	51	−0.46 (0.28)
	3	60	0.28 (0.28)
	4	74	0.53 (0.29)
Plant †	1	16	−0.24 (0.30)	.02
	2	20	−0.45 (0.29)
	3	23	0.25 (0.28)
	4	27	0.60 (0.29)

*Adjusted for sex, age, height, total energy (residual method), body mass index, physical activity, health status, sex/menopause status, and baseline grip strength.

^† Animal and plant protein intakes adjusted for each other as a continuous, energy-adjusted variable.

Lean Mass as a Mediator

In multivariable-adjusted models, baseline arm lean mass tended to be higher with greater total (β = 0.0027±0.002, p =.08) and animal (β = 0.0029±0.002, p = .06) protein intakes, and lower with greater plant protein intake (β = −0.0089±0.005, p = .05), though no associations were statistically significant. After adding baseline arm lean mass to the regression models for change in grip strength, results did not change (data not shown), indicating that lean mass likely does not account for the relation between protein and changes in grip strength.

Age-Stratified Analyses

In participants younger than 60 years ( n = 896), the mean annualized percent change in grip strength was positive (0.09±5.5 %/y). There were no significant linear trends for mean change in grip strength across quartiles of total and animal protein intakes ( Figure 1 ). There was, however, a borderline statistically significant trend for greater gain in grip strength with increasing plant protein intake ( p = .06), with the increase in strength in the highest quartile (1.11±0.40 %/y) significantly different from the loss (−0.45±0.38 %/y) in quartile 2 ( p = .03). Adjustment for arm lean mass and fruit and vegetable intakes did not change any associations (data not shown).

Figure 1.

Least squares-adjusted mean annualized percent change in grip strength (%/y) for quartiles of dietary intakes of total, animal, and plant protein for Framingham Offspring Cohort men and women aged ( A ) <60 years and ( B ) ≥60 years. Different letters indicate statistically significant differences at p < .05.

Among those aged 60 years or older ( n = 646), there was a mean loss in grip strength (−0.26±6.0 %/y). Higher total and animal protein intakes were associated with reduced loss of grip strength in these older adults (tests for linear trend p = .03 for both). While plant protein intake showed a similar trend, the association did not reach statistical significance ( p = .11). Adjustment for lean mass did not change these associations (data not shown). After adjusting for fruit and vegetable intake, trends were similar, although the p -values for total and animal protein reached the threshold of statistical significance (total protein p = .05; animal protein p = .05; plant protein p = .27).

Discussion

In our community-based cohort of adults, dietary protein intake was not associated with grip strength at baseline, but higher protein intake was associated with reduced loss of grip strength. This relation was most apparent for total and animal protein intakes among men and women aged 60 years or older, which is consistent with the prevailing evidence that muscle protein synthesis response to food intake diminishes with aging ( 21 ).

A recent systematic review and meta-analysis of trials of high protein oral nutritional supplements in older adults found evidence of a favorable effect on grip strength ( 22 ). There are, however, few population-based studies examining usual dietary protein intakes and muscle strength. Our findings agree with previous studies that indicate no cross-sectional association between dietary protein and grip strength ( 3–5 ). Most observational studies of dietary protein and longitudinal changes in muscle strength have examined lower extremity strength, and the results have produced little evidence of an association ( 7–9 ). Our longitudinal results are congruent with one study among older women enrolled in the Women’s Health Initiative clinical trials, in which the highest quintile of baseline biomarker calibrated protein intake lost less grip strength compared to the lowest quintile (0.45 vs 0.59kg/year) over 7 years ( 6 ). While we did observe statistically significant trends of reduced loss of strength with higher protein intakes in our sample of adults aged 60 years or older, the differences in loss between extreme protein intake quartiles were small (between 1% and 1.5% per year) and do not reach previously reported minimum clinically meaningful differences of 19% (approximately 6kg) ( 23 , 24 ). For this observational study of healthy community-based participants who were protein replete, we would not expect to see differences of this magnitude among our protein quartiles, which are in the range of usual dietary intakes. The differences between extreme quartiles that we did observe, however, approach the annual 1.5% loss of strength reported for adults in their 7th decade ( 25 ). Therefore, our results provide some evidence that increasing dietary protein intakes, even within the range observed in our cohort, may help prevent the expected loss of muscle strength experienced by aging adults.

It has been shown in older women that high animal protein diets result in greater net protein synthesis compared with high plant protein diets ( 26 ), likely because protein from animal sources has a complete amino acid profile. Thus, animal protein may be more beneficial for maintaining muscle mass. Some previous observational studies have supported this hypothesis ( 12 , 27 , 28 ), although a recent study among 2,762 community-dwelling older Chinese adults found that neither total nor animal protein intake were associated with change in skeletal muscle mass, while greater protein intake from vegetable sources was associated with reduced muscle loss ( 29 ). Furthermore, intervention studies examining the influence of animal protein intake on the effect of resistance exercise on muscle size do not support animal protein as more beneficial than plant protein ( 30 ). Our lean mass results are in agreement with these findings in that we found none of the different sources of protein to be associated with lean mass. Similarly, in our overall population, the protective association with change in grip strength that we observed was consistent for all protein sources. In our participants older than 60 years, however, only total and animal protein intakes were protective against loss of grip strength. Strength loss did tend to decrease with increasing plant protein intake in this older group, although the trend did not reach statistical significance, which is likely due to lower power to detect a trend in this subset of participants. Further studies are needed to clarify whether the influence of dietary protein on maintenance of muscle strength depends on protein source.

Although we did not have information on change in lean mass, our results suggest that muscle mass may not mediate the association between dietary protein and muscle strength. However, muscle mass is one of several factors that determine muscle strength ( 2 ), and there is emerging evidence that dietary protein may influence other characteristics of muscle besides mass. Dietary protein may play a role in insulin resistance and diabetes ( 31 ), which are associated with increased accumulation of intermuscular adipose tissue ( 32 ), a major determinant of reduced muscle strength ( 33 ). A recent study in young, healthy adults found that serum metabolites associated with dietary protein intake (branched chain amino acids) were positively associated with muscle quality (strength per unit of lean mass) ( 34 ). Finally, rats fed diets high in low quality protein had reduced muscle fiber contractility compared with those on animal protein diets ( 35 ). Although evidence is scant, it points to the possibility that protein may have benefits on muscle health beyond accretion of mass.

The current U.S. recommended daily allowance for dietary protein among adults aged above 18 years, published by the Food and Nutrition Board at the Institute of Medicine, is 0.8g/kg/d ( 36 ). This guidance, however, is based on data from young, male athletes and represents the minimum intake necessary to avoid a progressive loss of lean body mass, thus it does not achieve levels necessary to optimize muscle mass and strength and is likely not applicable to older adults ( 37 ). More recent guidelines based on improvement of clinical outcomes, namely muscle mass, strength, and physical function, recommend average daily protein intakes of 1.0–1.2g/kg/d for adults older than 65 years ( 38 , 39 ). Our data support increasing the protein recommended daily allowance for older adults (≥60 y) since individuals in the highest total protein intake quartile (median intake 94g/d; ~1.2g/kg/d) increased strength, compared with those in the lowest quartile (median intake 61g/d; ~0.8g/kg/d) who lost strength.

Our study has some limitations. Although quadriceps strength was measured around the time of our baseline assessment ( 40 ), we did not have information on longitudinal changes in lower extremity strength, which is more directly related to physical function ( 41 ). Grip strength is, however, correlated with lower extremity muscle strength and highly predictive of disability ( 42 ). FFQs do not measure actual protein intakes, yet previous validation studies have shown that the Willett FFQ can effectively rank individuals’ dietary intakes when used in large epidemiologic studies ( 14 ). Baseline FFQ, grip strength, and X-ray absorptiometry were not ascertained simultaneously, though it is unlikely that dietary intakes varied substantially between assessments. Finally, the Framingham Offspring cohort is composed exclusively of Caucasians, thus limiting generalizability to other race and ethnic groups. Despite these limitations, our study has several strengths. Our study population included large numbers of men and women representing a wide age range across the spectrum of adulthood. The longitudinal design established a temporal relation between dietary protein intake and change in grip strength, thus providing evidence supporting a causal relation. The Framingham Offspring cohort is well-characterized, enabling us to account for several potential confounding variables. Finally, we examined different sources of protein.

In conclusion, higher dietary intakes of total and animal protein, but not plant protein, were associated with decreased rate of muscle strength loss in men and women aged 60 years or older. Maintenance of muscle mass may not explain these relations. Our findings suggest that overall dietary protein and protein from animal sources may be important factors for sustaining physical function in old age, though more research is necessary to investigate whether maintenance of muscle strength due to dietary protein can help to prevent related clinical outcomes such as mobility impairment or falls. Further studies are needed to determine alternate mechanisms besides accretion of muscle mass through which dietary protein may influence muscle strength in older adults.

Funding

This work was supported by an unrestricted research grant from General Mills Bell Institute of Health and Nutrition; the National Institute of Arthritis and Musculoskeletal and Skin Diseases and the National Institute on Aging (grant numbers R01 AR53205 and R01 AR/AG41398); and the Heart, Lung and Blood Institute’s Framingham Heart Study (contract number HHSN268201500001I). The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.