Vincent Hou, BHSc1, Kenneth Madden, MSc, MD, FRCP(C)1,2,3
1Department of Medicine, The University of British Columbia, Vancouver, BC
2Centre for Hip Health and Mobility, The University of British Columbia, Vancouver, BC
3Gerontology and Diabetes Research Laboratory, Vancouver Coastal Health Research Institute, Vancouver, BCDOI: https://doi.org/10.5770/cgj.25.608
ABSTRACT
Sarcopenia, an age-associated skeletal muscle disorder characterized by muscle loss, is associated with disability in elderly populations. This literature review summarizes the impact of protein intake and supplementation on the indicators of severe sarcopenia—muscle mass, muscle strength, and physical function in community-dwelling older adults. We performed a literature search on PubMed, EMBASE, and MedLine, and included studies that evaluated the effects of protein intake with or without exercise intervention and on sarcopenia in community-dwelling older adults. Information regarding study participants, protein intervention, and sarcopenia-related outcomes were collected. Protein supplementation with or without exercise positively improves muscle mass, and aspects of muscle strength and physical function in sarcopenic and pre-frail older adults, while it elicited inconclusive effects in healthy populations. Greater dietary animal-based and soy-based protein diets can improve muscle mass in older adults. In conclusion, protein supplementation can improve muscle mass and reduce the risk of sarcopenia in sarcopenia and pre-frail older adults, while future studies should continue to investigate the effects of protein supplementation on indicators of sarcopenia in healthy older adults.
Key words: sarcopenia, community-dwelling, older adults, dietary protein intake
Sarcopenia is characterized by age-associated, progressive loss of muscle mass and physical function.(1) The European Working Group on Sarcopenia in Older People and the International Working group on Sarcopenia define severe sarcopenia as having lower skeletal muscle mass, muscle mass, and physical strength.(1) Previous research has demonstrated a higher prevalence of sarcopenia in older adults, due to decreasing hormonal activation, inadequate physical activity and nutrition, and lower neuromuscular junctional activity.(2–4) In fact, older adults over the age of 80 may lose up to 50% of their muscle mass.(2,3) Sarcopenia also acts as a significant determinant of disability: it increases the risk of falls, fractures, and mobility disorders, and is also correlated with higher risks of cognitive impairment and cardiometabolic comorbidities.(5,6)
There are no currently approved medications for sarcopenia treatment.(7) Instead, non-pharmacological therapies are often associated with the attenuation of muscle loss and improvements in muscle size and strength in older adults.(8) As reduced exercise capacity and higher prevalence of malnutrition is linked with older adults, an increasing number of studies report the impact of nutritional improvement and exercise intervention on sarcopenia, with the primary focus on protein supplementation with or without resistance exercise training.(8,9) From the current literature, multiple forms of protein intake interventions, with or without exercise intervention, are evaluated for their effects to attenuate muscle loss in the elderly population, including amino supplementation, whey protein intake, and an increase in an animal and protein-rich diet.(9) Therefore, this review aims to evaluate and provide a summary of evidence of dietary protein intake and protein supplementation and its effects on sarcopenia and the preservation of muscle mass, strength, and function in the community-dwelling elderly population.
For this literature review, we performed searches on the impact of protein supplementation in community-dwelling older adults within PubMed, EMBASE, and MEDLINE databases from 1975 to 2020. Please see Figure 1 for the search terms.
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FIGURE 1 Search terms for literature review assessing the effects of dietary protein intake on saropenia in community-dwelling older adults | ||
The titles and abstracts of the studies selected were screened. We included studies that evaluated the effects of increased dietary protein or any form of protein supplement, with or without other interventions, in improving the metrics of severe sarcopenia. Conference abstracts and studies that did not provide data on muscle mass, strength, or physical performance were excluded. Please see Figure 2 for the literature search flowchart.
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FIGURE 2 Literature search flowchart for review assessing the effects of dietary protein intake on saropenia in community-dwelling older adults | ||
After study selection, we extracted the following data: patient population, sample size, intervention, and sarcopenia-related outcomes (muscle mass, strength, and physical performance). Specifically, muscle mass was reported as total and appendicular lean mass, skeletal muscle index, or cross-sectional muscle area. Muscle strength was assessed based on parameters such as handgrip strength and knee extension strength. Physical performance was reported either as a Short Physical Performance Battery (SPPB) (balance, chair stand, and gait speed) or other tests including stair climb and timed-up-and-go.
Overall, our literature search yielded 29 studies including 19 randomized control trials, six prospective cohort studies, and four cross-sectional studies. The study populations of the 29 studies were heterogeneous, ranging from healthy, sarcopenic, pre-frail, obese, and diabetic participants. The major categories of interventions and variables assessed include amino acid and whey protein supplementation alone, nutritional supplementation combined with exercise intervention or electromyostimulation, and dietary protein supplement/dietary pattern assessment.
Six studies assessed the effect of unimodal protein supplementation on indicators of sarcopenia in community-dwelling older adults (Table 1). Three studies evaluated the effect of amino acid supplementation on muscle mass, muscle strength, and physical function. Solerte et al. assessed the effect of daily amino acid supplementation in sarcopenic older adults and found significant improvements in whole-body, arm, and leg lean mass, to the average values found in age-appropriate non-sarcopenic healthy controls after 16 months.(10) Similarly, Peng et al. discovered that 12 weeks of daily amino acid supplementation significantly improves mid-thigh cross-sectional area in pre-frail older adults compared to control participants, with no effects in handgrip strength and SPPB.(11) Lastly, a randomized controlled trial by Ellis et al. found that 16 weeks of amino acid supplementation can significantly improve total lean body mass and timed stair climb in healthy community-dwelling elderly participants compared to the control intervention.(12) However, they found no significant differences in quadriceps muscle volume or other physical functional tests, including gait speed and timed up-and-go test.(12)
TABLE 1 Studies with unimodal protein/amino acid supplementation
Three studies evaluated the effect of whey protein supplementation on muscle mass, muscle strength, and physical function. Through a randomized controlled trial, Kang et al. reported that 20 g of protein supplementation for 12 weeks only significantly improved total lean mass in healthy adults aged 50–64, but had no effects on muscle mass in participants >65 years old.(13) Furthermore, protein supplementation did not significantly improve muscle strength (grip strength or femoral muscle strength) or the SPPB.(13) On the other hand, Chanet et al. found that daily leucine-enriched whey protein medical nutrition drink can significantly improve higher appendicular and leg lean mass in healthy older adults.(14) However, there were no important between-group differences in total lean body mass, handgrip strength, and SPPB outcomes.(14) Lastly, Zhu et al. reported that two years of whey protein supplementation did not result in significant differences in muscle mass (appendicular skeletal muscle mass, upper/lower limb cross-sectional muscle area), muscle strength (handgrip and knee extension/flexion), and physical function (timed up and go test) in healthy older adults compared with isocaloric placebo intervention.(15)
The results suggest that amino acid supplementation effectively improves multiple aspects of muscle mass, including total-body, arm, and leg lean mass, in sarcopenic and pre-frail older adults over 3 to 16 months. However, amino acid supplementation had no significant effects on muscle strength and most aspects of physical function. In comparison, there are mixed findings regarding the effect of whey protein supplementation on muscle mass in community-dwelling elderly. However, whey protein alone is unlikely to induce any positive benefits in muscle strength and physical function in the healthy elderly population.
Overall, we identified 12 studies that evaluated the combined effects of nutritional supplementation and exercise or electromyostimulation intervention on various aspects of sarcopenia (Table 2). Exercise intervention in studies often included resistance exercises, such as biceps curl, chest press, and knee extension.
TABLE 2 Studies with protein/amino acid supplementation and exercise intervention or electromyostimulation
Four studies explored the role of amino acid supplementation and exercise intervention in improving muscle mass, muscle strength, and physical function. Yamamoto et al. randomized type II diabetic older adults into three groups: the amino acid + exercise intervention group, the exercise intervention group, and the control group. The study reported no significant differences in lean body mass, knee extension or grip strength, or gait speed between all groups post-intervention.(16) In contrast, Kim et al. found that sarcopenic older adults who received exercise and amino acid supplementation for 12 weeks significantly improved in leg muscle mass, knee extension, and maximum walking speed compared to the health education control group.(17) Furthermore, in a four-year follow-up study, they also compared the effects of all interventions (exercise + amino acid supplementation and either intervention alone) against sarcopenic older adults who were originally excluded from the study. The participants who received any one of the interventions had significant improvements in leg muscle mass, appendicular skeletal muscle mass, knee extension strength, and gait speed, compared to non-participating sarcopenic older adults.(18) Lastly, another randomized control trial reported that sarcopenic and obese older adults who received amino acid supplementation and resistance exercise intervention were over three times as likely to see improvements in knee extension strength and usual gait speed compared to the home education control group.(19) However, the study reported no significant differences in skeletal muscle index or grip strength between groups.(19)
In comparison, eight studies reported whey protein supplementation and exercise intervention and their effects on muscle mass, muscle strength, and physical function. Nilsson et al. conducted a randomized controlled trial in sarcopenic older men. The study found that participants who received both the protein supplementation and exercise intervention for 12 weeks had significant improvements in total muscle mass and appendicular lean mass, muscle strength (handgrip strength and leg press), and timed sit-to-stand test compared to pre-intervention.(20) There were no significant improvements in other functional tests or the overall SPPB score.(20) Similarly, Nabuco et al. reported that sarcopenic obese older women who received 12 weeks of both protein and exercise interventions had significant improvements in lower and appendicular lean soft tissue, muscle strength (chest press, preacher curl exercises, knee extension), and physical function (10-m walk and chair stand test) post-intervention.(21) Muscle mass was also significantly greater in the exercise and protein intervention group compared to the exercise intervention-only group.(21) In comparison, a Finnish study on community-dwelling sarcopenic older adults found that 12 months of protein supplementation in addition to home-based exercises resulted in no significant differences in grip strength and the SPPB compared to the exercise-only group.(22) However, the study reported poor compliance (45% compliance) throughout the intervention period.(22) Lastly, Kang et al. enrolled community-dwelling pre-frail or frail participants based on Fried’s criteria.(23,24) The study reported that participants who received both whey protein and exercise intervention for 12 weeks had significantly greater handgrip strength, gait speed, and five times longer chair stand time compared to those from the exercise-only group.(23)
Four studies evaluated the effects of exercise + protein interventions in healthy older adults. Kirk et al. reported that 16 weeks of whey protein supplementation in addition to resistance exercises did not significantly improve muscle strength (leg press, chest press, bicep curl) and physical function (SPPB) compared to exercise intervention alone.(25) Their follow-up study, recruiting more healthy older adults also found that protein supplementation and exercise intervention had no significant impact on muscle mass.(26) However, this study also cited a lack of compliance, with only 43% of participants completing the allocated intervention regimen.(26) Similarly, Galbreath et al. also reported that dietary protein intake and resistance exercise intervention on sarcopenia in overweight and obese older women did not significantly improve in muscle strength and physical function compared to isocaloric controls.(27) In contrast, Mori and Tokuda recruited healthy Japanese older women and randomized the participants into the resistance intervention + whey protein supplementation group, exercise-only, and protein-only groups.(28) After 24 weeks of intervention, the exercise + protein group had significant improvements in lower limb muscle mass, skeletal muscle index, and knee extension strength compared to the exercise-only group.(27) Exercise + protein group also had more significant improvements in upper limb muscle mass, grip strength, and gait speed, compared to the protein-only group.(27) Together, these results indicate that whey protein supplement + resistance exercise can improve aspects of sarcopenia more than either intervention alone.(27)
Lastly, Kemmler et al. evaluated the effects of protein supplementation and whole-body electromyostimulation (WB-EMS), an intervention using electric current to stimulate muscle growth, on sarcopenia in obese older males.(29) After 16 weeks of WB-EMS and whey protein supplementation, the intervention group significantly improved in fat-free and appendicular muscle mass, leg press strength, and gait speed compared to the control group.(29)
These findings demonstrate that amino acid supplementation and exercise intervention over three months significantly improved muscle mass, muscle strength, and physical function, particularly in sarcopenic older adults. Similarly, in sarcopenic and pre-frail older adults, most studies indicate that 12 weeks of whey protein supplementation combined with exercise intervention can improve muscle mass, muscle strength, and physical function compared to pre-intervention. However, when comparing protein + exercise intervention to exercise intervention alone, there are discrepancies in the improvements in muscle mass and strength, with generally fewer between-group differences in physical function. In healthy or non-sarcopenic older adults, there are incongruencies regarding the effects of whey protein supplementation and exercise on muscle mass, strength, and physical function. Lastly, whey protein supplementation combined with electromyostimulation can effectively improve parameters of sarcopenia in older adults.
Overall, five studies assessed the quantity of protein intake and its impact on aspects of sarcopenia in older adults (Table 3). One randomized trial evaluated the effects of daily ricotta cheese supplementation in sarcopenic older adults and found no significant differences in total muscle mass or handgrip strength between the intervention and control groups.(30) In comparison, in their cross-sectional study, Ten Haaf et al. reported that older adults with > 1 g/kg/day protein intake did not have significant improvements in handgrip strength and the SPPB score compared to participants with lower protein intake.(31) In contrast, in a prospective cohort study, Scott et al. assessed the effects of dietary protein intake on sarcopenia in healthy older adults, using cutoffs for protein intake based on the Australian Department of Health and Aging (64 and 81 g/day for men aged 51–70 and >70, respectively, and 46 and 57 g/day for women in the same age groups). The study found that participants who did not meet the recommended levels were associated with significantly lower appendicular lean mass at baseline and follow-up.(32)
TABLE 3 Studies assessing dietary protein intake
Unlike previous studies with recommended protein intake levels, Farsijani et al. conducted a prospective cohort study to assess the correlation between protein intake and muscle mass in ambulatory older adults.(33) The study found that older men with higher protein intake had higher total lean mass at baseline and follow-up.(33) However, the overall decline in lean mass during the follow-up was not associated with lower protein intake throughout the two years. There was no correlation between dietary protein intake and total lean mass in female participants.(33) Similarly, in a prospective study with ambulatory older adults, Otsuka et al. also reported that greater total protein intake led to lower odds of lean muscle mass decline in men, with no association reported in older women.(34)
The current literature demonstrates that there are inconclusive findings regarding the exact amount of dietary protein intake required to positively impact muscle mass, strength, and physical function in the elderly population. However, there is a general trend that increased dietary protein intake is associated with greater muscle mass in older men. However, similar trends were not observed in older women.
Three studies specifically evaluated the impact of an animal-based vs. plant-based protein diet on muscle mass (Table 3). A Taiwanese study reported that total and vegetable protein intake were significantly lower in healthy older adults with lower muscle mass, with participants with the lowest quartiles of intake having higher risks of developing low muscle mass compared to those in the highest quartile.(35) The study found no significant differences in animal-related protein intake between older adults with different muscle masses.(35) Similarly, another cross-sectional study found that Chinese participants in the highest quartile of vegetable protein intake lost significantly less appendicular skeletal mass over a four-year period than those in the lowest quartile of relative vegetable protein intake, with no effects on physical function.(36) Again, there were no significant associations between animal-based protein intake and muscle mass or physical function.(36) Compared to the two previous studies, a US study reported that animal protein intake was significantly associated with increased total and appendicular lean mass in older adults.(37) Participants in the highest quintile of total protein intake lost considerably less lean mass over three years compared to those in the lowest quintile of protein intake.(37)
Two studies also evaluated specific dietary patterns and their association with sarcopenia in older adults (Table 3). A cross-sectional study by Li et al. found that participants with the “mushroom-fruits-milk” diet (which also had a higher intake of legume and seafood) had the lowest prevalence rate of developing sarcopenia. In addition, the study reported significant associations between this type of diet and skeletal muscle index, grip strength, and gait speed.(38) Another cross-sectional study divided the participants’ diet based on three food groups: Mediterranean (olive oil, vegetables, whole grains, and fish), Western (tea, soy, fast foods, desserts, and sugars), and Mixed (animal proteins, legumes, potatoes, and refined grains).(39) The study found that participants in the highest tertile of the Mediterranean dietary pattern had lower odds of developing sarcopenia than those in the lowest tertile, and other patterns were not associated with sarcopenia.(39)
Overall, there are conflicting results when comparing the effects of plant-based protein vs. animal-based protein on muscle mass. Studies with an Asian population found that plant-based protein intake was associated with greater muscle mass, while animal-based protein intake was positively associated with muscle mass in American older adults. However, like previous studies, increased overall protein intake is generally negatively associated with lower muscle mass and developing sarcopenia in older adults. On the other hand, there is a wide distribution of dietary food groups and dietary patterns that may increase muscle mass. To summarize, a balanced diet consisting of fruits, vegetables, milk products, legumes, and seafood is positively associated with improved muscle mass and lower odds of sarcopenia development in older adults.
This literature review assessed the findings from studies on the impact of protein supplementation and dietary protein intake on various aspects of sarcopenia in community-dwelling older adults, including muscle mass, muscle strength, and physical function.
In general, we found that both amino acid and protein supplementation alone can improve muscle mass in pre-frail and sarcopenic community-dwelling older adults. In comparison, there were inconsistent findings between studies regarding the effects of nutritional supplementation on muscle mass in healthy older adults. However, protein or amino acid intervention alone was unlikely to elicit any benefits in muscle strength and physical function in healthy older adults.
Our study findings are consistent with previous literature, which shows that increased amino acids or protein supplementation could increase muscle protein synthesis and improve muscle mass, particularly in frail older adults.(40,41) In comparison, a previous systematic review that evaluated protein supplementation in healthy older adults has concluded that protein supplementation alone is unlikely to elicit positive effects in improving muscle strength and physical function.(42) In sarcopenic and pre-frail older adults, poor nutrition and chronic inflammatory conditions often cause attenuated protein metabolism and muscle synthesis, leading to more significant muscle loss.(43) Furthermore, pre-existing sarcopenia and pre-frailty further reduces physical activity in older adults, therefore further increasing the rate of muscle loss.(44,45) Therefore, protein supplementation may improve muscle mass in older adults with considerable muscle loss and less anabolic muscle gain.
Our literature review found that exercise intervention combined with amino acid or protein supplementation effectively improves muscle mass, muscle strength, and physical function in sarcopenic older adults compared to pre-intervention in sarcopenic and pre-frail older adults. In comparison, in healthy older adults, protein supplementation and exercise intervention elicited mixed results in muscle mass, muscle strength, and physical function.
In general, previous studies have shown that physical exercise can improve cardiorespiratory function, bone and muscle health, and reduce the risk of immobility in older adults.(46,47) In particular, resistance-based exercises can prevent muscle wasting and improve muscle strength, while effectively reducing frailty and enhancing mobility in older adults.(48) In line with our study findings, an earlier systematic review assessing the effects of nutritional supplementation and exercise intervention found that the combined interventions can positively impact lean muscle mass, knee extension strength, and gait speed compared to pre-intervention in sarcopenic older adults.(48) However, in healthy older adults, the effect of exercise intervention and protein supplementation on sarcopenia is limited, with previous literature reporting inconclusive results when assessing the effects of combined interventions on muscle mass, strength, and physical function.(42,49,50) These findings may be due to differences in baseline protein intake, activity level, and adherence to the exercise and protein interventions.
From studies within this literature review, there were inconclusive findings regarding the exact amount of dietary protein intake required to positively impact muscle mass, strength, and physical function in the elderly population. However, we found that overall increased levels of dietary protein intake is associated with greater muscle mass and lower odds of developing sarcopenia, particularly in older men. The National Academy of Science and the WHO established a Recommended Dietary Allowance of 0.8g/kg/day in older adults.(51,52) Nevertheless, recent reviews have suggested that higher levels of protein intake ranging from 1.0–1.5 g/kg/day may be more effective in preventing muscle loss in older adults.(53,54)
On the other hand, our literature review found mixed results when comparing vegetable-based proteins versus animal-based proteins and their effects on sarcopenia. Two studies with Asian participants found that plant-based proteins are more likely to improve muscle mass in older adults.(35,36) In contrast, one US study reported that animal-based protein intake is associated with increased muscle mass in older participants.(37) Previous research has revealed that animal-based protein contains higher levels of essential amino acids and is more easily digestible compared to plant-based proteins, leading to increased muscle protein synthesis and anabolism.(54) However, in studies with Asian participants, the most commonly ingestible vegetable-based proteins were soy products, which also have high essential amino acid profiles (with high levels of leucine) and near-equivalent protein digestibility compared to animal sources.(54) Consistent with our findings, a previous review also revealed when taken in adequate amounts, both animal-based and plant-based proteins can enhance and maintain muscle mass in aging populations, despite the differences in their anabolic properties.(55) Likewise, for dietary patterns, this review found that the Mediterranean diet, which consists of high amounts of fish protein and nuts, is associated with a lower risk of developing sarcopenia in older adults.(39) Many other studies have also cited the protective effects of the Mediterranean diet against muscle loss and frailty in the aging population.(56,57)
There are several limitations associated with this literature review. Firstly, we only conducted the literature search and only included studies from EMBASE, MEDLINE, and PubMed. We may have excluded literature in other languages or from other databases. Furthermore, the study participants’ baseline characteristics are not uniform. In particular, baseline dietary nutrition and physical activity were not assessed in several studies, making it difficult to draw conclusions based on the differences in the participant population. Lastly, the intervention and results are very heterogeneous in this study. Studies included varying protein supplementation amounts and exercise intervention durations, and they also measured outcomes in muscle mass, strength, and physical function differently. The variability in methods and outcomes can limit the comparability of the conclusions generated from the study findings.
In conclusion, in community-dwelling older adults, protein and amino acid supplementation can improve muscle mass in sarcopenia and pre-frail older adults, with variable effects in muscle strength and physical function. Furthermore, protein supplementation combined with exercise can further improve muscle mass, muscle strength, and physical function in the same group, with potentially additional beneficial effects than either intervention alone. However, there were inconclusive findings regarding the effects of protein supplementation with or without exercise intervention on muscle mass, muscle strength, and physical function in healthy older adults. Regarding dietary protein intake, higher protein intake and more spread protein intake distribution are associated with a lower risk of developing sarcopenia. Lastly, a higher intake of both animal-based and plant-based soy proteins can reduce the risk of sarcopenia. Future studies should continue to assess the impact of protein intake in community-dwelling older adults, with a particular focus on participant adherence and similar rates of baseline protein intake and physical activity, to generate a more comprehensive conclusion regarding the impact of protein and exercise interventions in healthy older adults. Furthermore, more standardized protein supplementation and exercise regimens can be implemented to improve comparability between studies and identify patterns in the future.
Not applicable.
We have read and understood the Canadian Geriatrics Journal’s policy on conflicts of interest disclosure and declare there are none.
This research did not receive external funding.
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Canadian Geriatrics Journal, Vol. 25, No. 4, December 2022