Myoprotective whole foods, muscle health and sarcopenia in older adults

Purpose of review Sarcopenia increases in prevalence at older ages and may be exacerbated by poor diet. Whole foods rich in specific nutrients may be myoprotective and mitigate the risk of sarcopenia. Here we review recent evidence published from observational and intervention studies regarding myoprotective foods and explore their benefit for the prevention and/or treatment of sarcopenia in older adults. Recent findings We found limited new evidence for the role of whole foods in sarcopenia and sarcopenia components (muscle mass, strength, physical performance). There was some evidence for higher consumption of protein-rich foods (milk and dairy) being beneficial for muscle strength in observational and intervention studies. Higher consumption of antioxidant-rich foods (fruit and vegetables) was associated with better physical performance and lower odds of sarcopenia in observational studies. Evidence for other protein- and antioxidant-rich foods were inconsistent or lacking. There remains a clear need for intervention studies designed to identify the role of whole foods for the treatment of sarcopenia. Summary Although evidence for myoprotective roles of dairy, fruit and vegetables is emerging from observational studies, higher level evidence from intervention studies is needed for these foods to be recommended in diets of older adults to prevent and/or treat sarcopenia.


INTRODUCTION
Sarcopenia, a progressive and generalized loss of skeletal muscle mass and function [1], is a common clinical problem in older adults [1].Sarcopenia prevalence increases with age [1,2], and depending on the definition applied, can reach 10-16% in general population and 16-60% in special patient populations [2].Sarcopenia is strongly associated with a range of adverse health outcomes, including co-morbid disease progression, increased risk of hospitalization, frailty, falls, disability [2], and poor quality of life [3].The high personal burden of sarcopenia is associated with a major societal burden manifested by substantial healthcare expenditure, especially when coupled with other age-related conditions [4].The epidemiology of sarcopenia points to a complex interplay between various risk factors, including diet poor in key nutrients and energy (malnutrition), low physical activity, and chronic conditions [2].The biology of sarcopenia is not fully elucidated, but there is increasing evidence for the role of cellular and molecular mechanisms governing ageing, such as oxidative stress, inflammation, and dysregulation of the protein synthesisbreakdown cycle in ageing muscle [5 && ].As there are currently no approved drugs for sarcopenia [6  & ], a healthy lifestyle comprising a high-quality diet and resistance exercise have been championed as the most effective strategy for sarcopenia prevention and treatment [7,8 && ,9

&& ,10
& ].The nutrition-sarcopenia research field has grown substantially since the implementation of the sarcopenia concept 30 years ago [11], and several nutrition approaches have been adopted to test their effectiveness in mitigating sarcopenia; from a single nutrient to a whole food and a whole diet approach [9

&& ,12
& ].Although two recent consensus guidelines for sarcopenia diagnosis, prevention, and management [8 && ,13 && ], have endorsed nutritional assessment and the promotion of balanced diets with sufficient high-quality nutrients, such as protein for the prevention of sarcopenia, these recommendations were mostly supported by observational epidemiological findings.For example, the Asian Working Group for Sarcopenia consensus guidelines [8 && ] recommend a daily protein intake of !1.0 g/kg body weight (BW) for healthy older adults and !1.2 g/kg BW for those with sarcopenia that should come primarily from diet, and where not possible, from protein supplementation with amino acids (e.g., leucine) or oral nutritional supplement (ONS) containing leucine or its metabolites.
Our last systematic evaluation of whole foods hypothesized to be beneficial for muscle and sarcopenia (myoprotective) in adults aged !50 years found benefits for higher consumption of protein-rich foods (lean meat, nonliquid dairy) for muscle mass, and higher consumption of antioxidant-rich foods (fruit and vegetables) for better muscle function [14].Although this review included 28 studies (19 observational) published until March 2020, the evidence summary was largely based on cross-sectional studies.Our more recent narrative summary of the role of nutrition (including whole foods) in sarcopenia incidence focused on only prospective and intervention studies in middle-aged (<60 years) and older adults (60-70 years) [9

&&
].The scope of the present review was therefore to provide an overview of the latest evidence (published from April 2022 to November 2023) from observational and intervention studies examining the associations of whole foods with sarcopenia and its components (muscle mass, strength, and physical performance), alone or with exercise, in older adults (aged !55 years).Whole foods consumed habitually are grouped into two broad categories, protein-rich and antioxidant-rich whole foods (Fig. 1).Practical implications of new evidence (or lack of it) are also briefly discussed.

Myoprotective protein-rich foods
Adequate consumption of protein-rich foods may help to combat imbalance between muscle protein synthesis (MPS) and breakdown with ageing [15], especially foods providing high-quality proteins with higher content of essential amino acids (EAA) such as leucine.Protein-rich foods that have a high Digestible Indispensable Amino Acid Score (!75), a metric used to evaluate the protein quality in a food, meal, or diet, come from both animal and plant sources.These include dairy, meat (red and white), most fish/shellfish, eggs, legumes, nuts, and soybean products [16].Our latest evidence summary of prospective and intervention studies investigating the effects of protein-rich foods on sarcopenia incidence has found limited and mixed evidence in both younger (aged <60 years) and older adults (aged 60-70 years) [9

&&
]. Below we consider newer evidence from a few recent observational and intervention studies with protein-rich foods (milk and dairy products, meat, fish/shellfish) in relation to sarcopenia components.

Milk and dairy products
Current dietary recommendations for overall health recognize the contribution of milk and dairy products (cheese, yoghurt) to a healthy diet in the general population.For example, a longevity-associated dietary pattern high in milk and dairy products, vegetables, nuts, and legumes (but low in refined grains and processed meat) was associated with a 10year gain in life expectancy in middle-aged and older adults in UK Biobank [17 && ].A high content of leucine, a pro-anabolic branched-chain amino acid that activates the mammalian target of rapamycin complex 1 (mTORC1) signalling pathway [18], has made milk an attractive whole food for potential myoprotection.Other bioactive components in milk have also gained attention, such as lipids and proteins residing within the milk fat globule membrane (MFGM) because of their

KEY POINTS
Sarcopenia increases in prevalence at older ages and may be exacerbated by poor diet.
Conversely, certain nutrient-rich whole foods may be myoprotective and mitigate the risk of sarcopenia.
Recent evidence from observational and intervention studies suggests that higher consumption of protein-rich (dairy) and antioxidant-rich whole foods (fruit and vegetables) may protect against loss of muscle strength and physical performance.
Although some nutrient-rich foods appear to be myoprotective in older adults, higher level evidence from intervention studies is needed for them to be recommended to prevent and/or treat sarcopenia.apparent antioxidative, anti-inflammatory, and immunomodulating potentials [19].
Only two recent studies explored the relationship between milk (bovine and deer) consumption, muscle strength, mass, and physical performance.In the Shimane CoHRE cross-sectional study of 656 Japanese older adults (mean age 75.6 years, 62.7% women), a higher consumption of milk, yoghurt, cheese was linearly associated with greater grip strength, and faster walking speed in women, but not in men.No associations with muscle mass were found in either sex [20].Observational studies with repeated assessment of dairy intake to examine prospective associations with sarcopenia and sarcopenia components are rare, therefore the findings from the Medical Research Council National Survey of Health and Development study are important [21].The study examined the consumption of total, fullfat, and reduced-fat milk each categorized in thirds (T1 (lowest) and T3 (highest) g/day) from age 36 to 69 years in association with low grip strength (probable sarcopenia) in later life, and grip strength (GS) decline from age 53 to 69 years in 1340 men and 1383 women [21].The results were mixed, and only T2 (58.76-145.25 g/day) of reduced-fat milk was associated with 40% lower odds of probable sarcopenia at the age of 69 years.In multilevel models, only T3 of total milk (!237.5 g/day) was associated with 1.82 kg stronger GS in midlife (age 53 years) in men compared with T1 ( 152.0 g/day), but not with GS decline over time.Although it could be inferred from this study that higher milk consumption may be beneficial for muscle strength in middle-aged men, its role in muscle health in late life needs further confirmation in other cohorts [21].
Two recent intervention studies found the benefits of a milk protein snack with high content of MFGM [22] and deer milk (as bovine milk alternative) [23 & ] for muscle function in older adults.We recently hypothesized about bovine milk myoprotecive potential beyond pro-anabolic effects of milk proteins, whey and casein [24].These include antioxidative, anti-inflammatory, and immunomodulating capacity of milk bioactive components, some of which constitute the MFGM.MFGM is a unique and complex structure of mainly lipids and FIGURE 1.Evidence summary from recent observational and intervention studies using a whole food approach for prevention and treatment of sarcopenia (sarcopenia components) in older adults.Each circle represents a study as described in the figure legend (13 unique studies, four conducted in women only).Arrows connect each food group with a study circle for a specific sarcopenia component, with some studies having multiple components.Some evidence was found for benefits of protein-rich foods (milk and dairy) for muscle strength, and antioxidant-rich foods (fruit and vegetables) for physical performance and lower odds of sarcopenia.Created with BioRender.
proteins that encases fat globules in mammal milk [19].MFGM structure includes phospholipids, glycolipids, and glycoproteins that have important functional roles for human health [19,25].The effects of a milk snack (containing !23 g of protein and 3.6-3.9g of MFGM) on physical performance (5-chair stands) was investigated in women aged !70 years at risk of sarcopenia (i.e., SARC-F tool score of 2) and dietary protein intake <1.2 g/kg BW/day in a 12-week intervention study.The intervention group consumed the milk snack daily with their habitual diet as either dairy protein powder (a serving of 30 g) or chocolate milk shake (a serving of 250 ml), and all participants were taught a fivemovement lower body exercise routine to perform daily [22].No differences in 5-chair stands were observed postintervention between the groups, and a small improvement of 2 s in both groups was attributed to exercise.However, there was a 0.8 points improvement in Short Physical Performance Battery (SPPB) in the nutrition intervention group (an effect size of 0.42), which was mainly due to improvements in balance.No change was observed in walking speed and grip strength [22].
Deer milk has a unique nutritional profile characterized by high contents of protein, B-vitamins, vitamin A, calcium, zinc, magnesium, and shortand medium-chain fatty acids, and low content of lactose [26], which may address potential nutritional deficiencies in older adults.An 11-week intervention study contrasted the effect of deer milk (DM) and oral nutritional supplement (ONS) on muscle mass and physical performance in 120 women aged 65 to 80 years.Twenty-nine percent of women had protein intake <1 g/kg BW/day and 38% were at risk of malnutrition [23  & ].The study observed a significant between group difference in percentage change in muscle mass (DM 1.68 AE 2.77% vs. ONS À0.18 AE 2.81%) in women with BMI >25 kg/m 2 and in grip strength (DM 10.6 AE 23.6% vs. ONS À5.03 AE 18.1%) in women with BMI <25 kg/m 2 .The results suggest that baseline nutritional status and BMI may modulate DM response to muscle mass and strength.This is the first study to investigate the effectiveness of DM for muscle health in older adults [23 & ].Although DM compliance was higher than in the ONS group, more women in DM group reported gastro-intestinal discomfort, which should be considered when designing larger trials.

Meat
Red meat is a nutrient-dense food and a source of high-quality protein, beneficial fatty acids (monounsaturated fatty acids, MUFA), and several micronutrients (B-vitamins, iron, zinc) essential for optimal health of in older age.Red meat contains all eight EAA required in adulthood, and in combination with other nutrients may play an important role in supporting optimal health [27].Conversely, nonlean red meat, and especially processed red meat, has a relatively high content of saturated fatty acids with minimal amounts of polyunsaturated fatty acids (PUFA), high sodium and preservatives content that may impact on sarcopenia (e.g., via effects on inflammation and oxidative stress) [5

&&
]. Recent studies have examined associations between meat and processed meat with sarcopenia components.The Nurses' Health Study investigated prospective associations between habitual consumption of red meats (total, unprocessed, and processed) and low muscle function in 85,871 women aged !60 years at baseline in 1992 [28 & ].Meat intake was evaluated nine times from 1980 to 2010, and muscle function six times from 1992 to 2014.During 22 years of follow-up, the relative risk of low muscle strength and reduced aerobic capacity (defined as having difficulty to walk one flight of stairs and walking several block or miles, respectively) was raised by 19% and 22% respectively for every one serving/day increase in processed meat intake [28 & ].

Fish and seafood
Fish and seafood as a part of healthy and sustainable diet are source of high-quality protein, vitamins, minerals, and fatty acids that may be beneficial for muscle health [29].However, there have been a few recent studies investigating the association between fish consumption and sarcopenia.A higher intake of fish (!15.3 g/day) was associated with a 40% (95% CI: 0.42, 0.82) lower risk of low lean mass and correlated positively with muscle mass in a cross-sectional analysis of 2,192 women aged !65 years from the Korean National Health and Nutrition Examination Survey (2008-2011) [30].No associations were observed in 1620 men.Although women consumed less dietary protein than men (45 vs. 60 g/day), the authors postulated that the beneficial effects of fish protein on muscle mass could be attributed to n-3 PUFA possibly stimulating MPS in a sex-specific manner when protein intakes are not optimal [30].However, debate is still ongoing about the mechanisms by which n-3 PUFA may improve muscle health and enhance anabolic response in older adults [31].
In summary, we have found limited new evidence about the role of protein-rich whole foods such as dairy, meat, and fish in sarcopenia (sarcopenia components) in older adults.There is some evidence suggesting a higher consumption of milk (including deer milk) may be beneficial for muscle strength; conversely a higher consumption of processed meat appears detrimental for muscle strength and function in older women.Furthermore, there is a lack of clinical trials with whole foods to improve components of sarcopenia and prevent muscle health decline, as well as paucity of prospective observational studies with repeated measures of these foods for prevention of sarcopenia in older adults.

Myoprotective antioxidant-rich foods
The health benefits of antioxidant-rich foods (e.g., fruit, vegetables, legumes, nuts, seeds, soy, olive oil) have been well documented.As a crucial part of a healthy, balanced diet, a higher consumption of a variety of these foods have been linked to positive health outcomes, including longevity and reduced risk of chronic diseases [17 && ,32].Fruit and vegetables are a perfect example of whole foods low in energy but dense in nutrients (vitamins, minerals, protein, dietary fiber) and nonnutrients known as phytonutrients [32].Phytonutrients are biologically active compounds that have several beneficial properties, including antioxidant, anti-inflammatory, and antibacterial properties [32] within a healthy, balanced diet.Higher habitual consumption of fruit and vegetables may exert beneficial effects by increasing the antioxidative capacity of the diet and counteracting the inflammatory response in ageing muscle [5

Fruit and vegetables
We have previously reported on findings from studies demonstrating consistent, positive associations between higher consumption of fruit and vegetables and muscle function in adults aged !50 years (six observational and one intervention study) [14].Evidence for other antioxidant-rich food (e.g.nuts and legumes) was limited and inconclusive.More recently we have summarized prospective and intervention studies that have examined the effects of whole foods on risk of incident sarcopenia (sarcopenia components): higher consumption of fruit and vegetables was most consistently positively associated with muscle function in mid-adulthood (<60 years), whereas low consumption was associated with poor muscle health in this age group [9

&&
].In that review, prospective evidence in young-older adulthood (60-70 years) was the most consistent for positive associations between fruit consumption and muscle function.No associations were found between fruit and vegetables consumption and other components of sarcopenia [9 && ].There are few studies of the role of antioxidantrich foods published more recently.In a large crosssectional study of 5418 Chinese adults (53% women) aged !65 years from the Study on Global Aging and Adult Health, meeting the recommendations for fruit and vegetables intake (!2 and !3/ servings/day, respectively) was associated with 31% lower odds of sarcopenia, which were further reduced by 3% if combined with physical activity [33].In a 6-month feasibility trial with 91 older adults (46% women) aged 68 AE 8 years, addition of 100 g/day of dried fruit to participants' habitual diet otherwise low in fruit consumption resulted in no significant change in physical performance (Health ABC SPPB) and there was no change in lean nonfat and nonbone lean mass [34].
In the latest systematic review and meta-analysis of 28 studies (19 observational/13 cross-sectional and nine intervention studies published between 2000 and 2020), the impact of antioxidant-rich foods (fruit, vegetables, beans, nuts, seeds, tea, cacao, and oils) and antioxidant supplements on muscle health was investigated in adults aged !55 years [35  & ].Based on largely cross-sectional evidence, the authors found benefits of higher fruit, vegetables, and nuts consumption for sarcopeniarelated outcomes.Specifically, higher intakes of fruit, vegetables, and nuts were associated with better muscle mass, grip strength, measures of muscle agility, and mobility.Meta-analysis of a few eligible intervention studies revealed better physical performance (i.e., faster time to complete five chair stands in seconds) in intervention groups (fruit and vegetables; Mg, vitamin E with vitamin D and protein supplements), a mean difference (MD) of À1.11 (95% CI: À1.70, À0.51), and greater muscle strength (grip strength in kg), a MD of 1.02 (95% CI: 0.60, 1.44) compared with controls.Only five observational studies (four cross-sectional) examined the risk of sarcopenia in relation to antioxidant-rich foods or dietary patterns with higher intake of antioxidant foods, and only three found lower risk of sarcopenia with higher intake of these foods.However, there were no intervention studies examining the effect of antioxidant-rich foods on sarcopenia [35 & ].The lack of intervention studies with whole foods for muscle health was also noted in a recent review of individual trials, large observational studies, and meta-analyses investigating lifestyle factors in prevention of sarcopenia published in the last 10 years (2011-2022) [36].
Taken together, there is a need for well designed, long-term intervention studies with diet/whole foods or those assessing the added value of whole foods supplementation to exercise intervention in a diverse population of older adults to better validate the mechanisms of action of each nutrition intervention [14,36].
In summary, recent studies have added to the evidence that higher intakes of antioxidant-rich foods, and particularly fruits and vegetables, are associated with lower odds of sarcopenia, better muscle strength and physical performance in older adults.However, this evidence is based on mostly observational studies, whilst intervention studies with antioxidant-rich whole foods for prevention of sarcopenia are lacking.

Multiple whole foods
Associations between multiple whole foods and sarcopenia (or sarcopenia components) were investigated in three recent observational studies.In a cross-sectional study of 9,080 Japanese older adults (mean age 74 AE 5.6 years; 56% women) from the National Center for Geriatrics and Gerontology-Study of Geriatric Syndromes, lack of diversity of high-protein foods (meat, fish/shellfish, eggs, milk, soybean, potatoes) was associated with 47% higher risk of sarcopenia [37].This suggests that a variety of protein-rich foods should be consumed to reach myoprotection and sufficient supply of EAA.In another cross-sectional study of 1,059 Chinese adults (mean age 67.9 AE 7.6 years; 74% women) residing in Beijing, higher frequency of daily consumption of fruit, nuts, and dairy was associated with lower prevalence of sarcopenia [38].Moreover, in a study of 801 Korean older adults (age range 70-84 years; 52% women), the highest quartile of intake of protein-rich foods (meat, fish, eggs, legumes), and vegetables was associated with 50% (95% CI: 0.26, 0.97) and 72% (95% CI: 0.13, 0.59) reduced odds of prevalent sarcopenia, respectively [39].No associations were found for fruit, grains, or dairy.
Based on these studies, a combination of different protein-rich and antioxidant-rich whole foods may be needed to enhance diet diversity and quality to enable healthy muscle ageing and reduce the risk of sarcopenia.

Myoprotective protein-rich foods
Intervention studies assessing the effects of whole foods (with or without exercise) on sarcopenia (sarcopenia components) are rare (reviewed in [7,14,36]).Even rarer are this type of interventions in older adults with diagnosed sarcopenia.In their latest review, Calvani et al. [7] have listed 12 ongoing registered clinical studies investigating nutrition interventions for sarcopenia, of which only three were with whole foods (lean ground meat, fermented milk, virgin olive oil).We have found only one recent intervention study that tested the effect of protein-rich foods in older adults with sarcopenia symptomatology.

Eggs
Because of its relatively low cost, high digestibility, and high content of EAA, higher consumption of egg white may increase the anabolic potential of high-quality diets for better muscle mass and function, especially in older adults at risk of malnutrition.In a recent randomized controlled trial pilot involving 29 women aged !60 years at risk of food insecurity, low-protein diet (<0.8 g/kg body weight/ day), and probable sarcopenia, a daily supplement of egg white (providing 20 g of protein) versus isocaloric maltodextrin supplement (control group, n ¼ 13) for 6 months resulted in no between-group differences in muscle mass and function [40].However, grip strength, number of arm curls, and protein intake improved significantly from baseline in the intervention group but not in the control group [40].

Myoprotective antioxidant-rich foods
There are no recent studies testing the effect of antioxidant-rich whole foods for sarcopenia in older adults, leaving a big gap in knowledge, even when upcoming trials are considered [7,12 & ].

CONCLUSIONS AND PRACTICAL APLICATIONS
We have summarized recent evidence from observational (cross-sectional and prospective) and intervention studies investigating the role of whole foods in the prevention and treatment of sarcopenia (sarcopenia components) in older adults.Findings  , [37][38][39] are presented in Fig. 1.Overall, we have noted limited new evidence that has examined myoprotective potential from protein-rich and antioxidant-rich foods.There is a marked lack of clinical trials and prospective studies.There is some limited evidence for benefits of higher milk consumption for muscle strength, and greater fruit and vegetables consumption for muscle function.However, this evidence is mostly from observational studies.Most notably, there is a lack of nutrition interventions with whole foods in older adults with sarcopenia, including in upcoming clinical trials [7,12  & ].The strength of evidence from the presented new studies should be considered in the context of their design, duration, population under study, nutrition assessment, collinearity of foods, confounding factors (for observational studies), and the type, amount, and frequency of nutrition intervention (for intervention studies).For example, there were six unique studies (four observational of which two prospective) with protein-rich foods for prevention and risk reduction of sarcopenia [20,21,28 & ,30].Three were conducted in women only with some women being at risk of sarcopenia and malnutrition.There were only two new unique studies with antioxidant-rich foods, of which one was intervention study showing no effect on muscle performance in men and women [34].All studies reported on agerelated conditions (self-reported or from medical records), medication intake, or malnutrition status to characterize the population under study.Regardless of differences across the studies, the majority of participants (>50%) had at least one or more conditions, typical for older adults living in the community [41].Other evidence presented here was collated from recent narrative and systematic reviews with meta-analyses [7,9 Although evidence for myoprotective roles of dairy, fruit and vegetables is emerging from observational studies, higher level evidence from intervention studies is needed for these foods to be recommended in diets of older adults to prevent and/or treat sarcopenia.
Rolland Y, Dray C, Vellas B, Barreto PS.Current and investigational medications for the treatment of sarcopenia.Metabolism 2023; 149:155597.This is the latest comprehensive review of drug trials for sarcopenia, including some promising recent molecular investigations.

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,36], highlighting the dominance of cross-sectional studies, heterogeneity of intervention studies with whole foods, and the lack of interventions for treatment of sarcopenia.
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