Protein for Life: Review of Optimal Protein Intake, Sustainable Dietary Sources and the Effect on Appetite in Ageing Adults

In the UK, it is projected that by 2035 the majority of the population will be aged 40 or older [ 1 ]. The considerable size of this cohort has seen increasing interest from policy officials in utilizing dietary guidance to maintain or improve their health and wellbeing to promote healthy ageing. Adequate intake of protein is one of the key nutritional factors to maintain independence, predominantly by preventing loss of muscle mass and strength (sarcopenia), frailty and associated comorbidities in later life [ 2 , 3 , 4 ]. At present, the food sector is failing to identify and directly address the needs of this ageing population, with affordable, palatable and practical food solutions. It is debatable at what exact point in life muscles start to age. A gradual decline in muscle mass is observed from the third decade of life [ 5 ], with a 30–50% decrease reported between the ages of 40 and 80 [ 6 ]. Muscle strength is correlated with muscle mass and rapidly declines after the age of 50 [ 7 , 8 ]. The beginning of the fourth decade of life might therefore be interpreted as the time when muscle ageing process begins and for this reason it is the optimal time for implementing appropriate dietary changes, to prevent or delay the onset of sarcopenia. Accordingly, throughout this review an ‘ageing adult’ is used to refer to a person aged 40 and older. Previous work has focused on identifying the optimal protein amount, timing and type of protein for sarcopenia prevention. A number of studies have found that intake exceeding the Recommended Daily Allowance (RDA) may be preferential in preserving muscle mass and functions in ageing adults [ 3 , 9 , 10 , 11 , 12 ]. In addition, the pattern of protein consumption was suggested to be of greater importance than the total daily amount consumed [ 13 ], which will be discussed in the next section. The evidence from these studies is however limited to investigating the effects of different types of animal proteins on muscle health [ 14 , 15 ], and the effects of plant proteins (other than soy) have not been adequately studied. Plant-based nutrition has received much attention in the past decade [ 16 , 17 ]. The ever-growing demand for foods naturally rich in protein is part of an ecological debate around whether more sustainable sources should be encouraged [ 18 ]. The high proportion of animal-protein consumption in developed countries [ 19 ] raises both health and environmental concerns. Firstly, dietary patterns characterised by a high intake of animal protein have been associated with increased risk of obesity, diabetes, cardiovascular disease mortality and some cancers [ 20 , 21 , 22 , 23 ]. However, it has to be stressed, that dietary patterns describe diet as a whole and it cannot be concluded that all components (e.g., meat, fish, eggs, dairy) of animal-based patterns have an equal, detrimental effect on health. Secondly, animal-protein consumption requires large areas of dedicated land, water, nitrogen, and fossil energy for production and transportation [ 24 , 25 ]. The result is the emission of large amounts of greenhouse gases (GHG) [ 26 ]. The health benefits of plant-proteins (as a more sustainable alternative) in sarcopenia prevention have yet to be investigated extensively. Furthermore, the effects of plant proteins on muscle protein synthesis (MPS) were scarcely investigated in the context of appetite, a significant risk factor for malnutrition and subsequent loss of muscle tissue [ 27 ]. It has not been yet established whether plant proteins trigger similar appetite-related responses in underweight, normal weight and overweight individuals while they age. Addressing this research gap is crucial to assess whether nutritional strategies can maximise the nutritional status of an ageing adult and whether increasing protein consumption chronically reduces energy intake, thereby increasing the risk of malnutrition. More generally, insight of this kind may help consumers to make healthy food choices and will inform the development of nutritionally balanced products that promote healthy ageing. The purpose of this review is threefold: (1) to summarise evidence regarding the optimal quantity and daily distribution of protein intake in ageing adults; (2) to present current knowledge about sustainable protein intake in the context of appetite control; and (3) to identify the areas for future research and challenges in introducing novel food solutions to consumers.

Apart from the total daily intake, per-meal protein quantity and daily frequency of protein ingestion have also been shown to play an important role in preserving muscle mass and function. It is estimated that consumption of two to three meals a day, each containing ~25–30 g of high-quality protein, is optimal for the stimulation of 24-h muscle protein synthesis (MPS) in healthy adults [ 38 , 39 , 40 , 41 , 42 ]. This approximate quantity is thought to be sufficient, both for younger and healthy older adults [ 39 ]. Interestingly, ‘the more, the better’ approach is not necessarily optimal. Moore and colleagues [ 43 ] investigated the per-meal threshold in relation to body weight and age. In this study, protein utilisation plateaued after the ingestion of 0.24 g of whey and egg protein/kg/bw in young men (~22 years) and after 0.40 g/kg/bw in older men (~71 years) [ 43 ]. Similar findings were reported in an acute feeding study by Symons and colleagues [ 39 ] who compared the effects of 30 g of lean-beef protein/meal to 90 g/meal ingestion on MPS in young (35 ± 3 years) and older adults (68 ± 2 years) and found there was no additional benefit of increased protein consumption in either age category. The estimated per-meal threshold after consuming a plant protein-rich meal is still unknown, particularly in ageing adults [ 44 ]. Some studies argue that consuming a higher dose of protein on one daily occasion (pulse feeding) can stimulate a higher anabolic response than smaller doses across multiple meals [ 45 , 46 , 47 ]. Arnal and colleagues [ 45 ] reported that during the trial, women (mean age 68 ± 1 years) who consumed 79% of daily protein at noon, 7% in the morning and 14%% in the evening had improved nitrogen balance, when compared to women who consumed their protein spread over four meals (21.5 ± 0.5, 31.2 ± 0.2, 19.1 ± 0.5, 28.3 ± 0.5% of daily protein intake). However, none of these four meals contained the required bolus of 25–30 g protein per serving, which could be a potential cause why the spread pattern treatment was less effective. Reports by Bouillanne and colleagues [ 46 , 47 ] were in line with Arnal’s findings, suggesting that pulse feeding was more effective in improving lean mass index in older adults. However, since participants in these studies were recruited from very old (mean age 84.1 years) hospitalised patients at risk of malnutrition the results should be cautiously interpreted and cannot be generalised to younger, healthy adults. In most Western societies, the daily pattern of dietary protein ingestion is skewed regardless of age or sex, with the lowest amount of protein being consumed in the morning and the greatest in the evening meal [ 48 , 49 , 50 , 51 ]. As shown in a British cohort study that has followed the dietary intake of adults aged 36 years for 17 years, the protein content of meals has gradually shifted toward the evening [ 48 ]. Although these results refer to years 1982–1999, evidence suggests, that this trend has been sustained because it is mirrored in data collected more recently from other countries. Data from U.S. National Health and Nutrition Examination Survey (NHANES) [ 49 ] indicate that in 2006 the average protein intake (g/meal) among women aged 51–71 year age group was 11.9 ± 0.4 (breakfast), 17.9 ± 0.5 (lunch) and 30.4 ± 0.7 (dinner) with snacks constituting 7.4 ± 0.3 [ 49 ]. The intake (g/meal) in men was higher and accounted for 15.8 ± 0.5, 23.2 ± 0.8, 43.5 ± 1.0 and 10.5 ± 0.5, respectively [ 49 ]. Results from this study have also confirmed that the same pattern was observed in a ≥71 years group. However, the amount of protein consumed in each meal was lower in both sexes, in comparison to the younger age group [ 49 ]. Regarding the population of the very old community-dwelling adults, the pattern of daily protein distribution appears to peak at mid-day. The Newcastle 85+ study [ 52 ] revealed that the highest amount of protein in this British cohort was consumed at lunch time, accounting for ~35% (around 20 g) of daily protein intake, followed by dinner ~21% (12 g), and in the period between lunch and dinner ~17% (10 g). The remaining protein were consumed at two consecutive morning occasions ~22% (13 g, combined), and late evening meal. The commonly observed uneven pattern of protein ingestion in older adults suggests a potential risk of insufficient stimulation of MPS, even when RDA on a daily basis is being met. Meaning, the stimulation with a meal containing ~25–30 g of protein occurs only once a day, during the main meal (lunch or dinner). As suggested by Bollwein and others [ 13 ], the protein distribution at older age is of higher importance than the total daily amount per se. In this study, the recommendation of 0.8 g/kg/bw was exceeded by all participants (>75 years), even those from the lowest quartile of protein intake. No differences were observed between frailty status and daily protein intake. However, those with a more uneven dist

There is debate about the optimal source of protein and numerous quality assessment measures have been proposed [ 56 ]. The most commonly applied method to assess protein quality involves the calculation of a Protein Digestibility Corrected Amino Acid (PDCAA) Score, or Digestibility Indispensable Amino Acid (DIAA) Score [ 57 , 58 ]. In general, animal-based foods are recognised as a superior source of protein because they have a complete composition of essential amino acids, with high digestibility (>90%) and bioavailability [ 59 ]. Animal proteins have higher PDCAA scores than plants, suggesting greater efficiency in muscle anabolic processes [ 58 ]. For example, proteins found in milk, whey, egg, casein and beef have the highest score (1.0), while scores for plant-based proteins are as follows: soy (0.91), pea (0.67), oat (0.57) and whole wheat (0.45) [ 58 ]. However, proteins do not occur in foods in isolation and the entire food matrix should to be considered when health benefits are evaluated [ 56 ]. Apart from protein, animal-based foods provide heme-iron, cholecalciferol, docosahexaenoic acid (DHA), vitamin B12, creatine, taurine, carnosine and conjugated linoleic acid (CLA); all compounds not present in plant-based foods [ 60 ]. Thus, moderate consumption of high-quality unprocessed animal-based foods should not be discouraged entirely. On the other hand, foods of animal origin contain saturated fatty acids (SFA). Although unfavourable effects of SFA on health should not be generalised to all animal-originated products (e.g., dairy or fish oil), there is a large body of evidence that processed meat (also high in SFA) is associated with increased risk of cardiovascular disease, dyslipidaemia and some forms of cancers [ 61 , 62 , 63 ] and is classified as group 1 carcinogen [ 64 ]. Plant proteins are often described as incomplete, due to the insufficient amounts of all nine essential amino acids [ 59 ]. Although protein content and amino acid composition vary between plant species, in general, protein found in legumes are limited in methionine and cysteine; cereals (lysine, tryptophan); vegetables, nuts and seeds (methionine, cysteine, lysine, threonine); seaweed (histidine, lysine) [ 65 ]. In addition, the digestibility and bioavailability of plant proteins is lower than those from animal sources, due to the high content of dietary fibre and plant bio-compounds (also called phytochemicals), e.g., trypsin inhibitors, phytates, saponins or tannins [ 66 ]. Interestingly, regarded in the past as anti-nutritional compounds, phytochemicals are being now increasingly associated with beneficial effects, e.g., regulating blood glucose level, improving lipid profile and reducing the risk of certain cancers [ 67 ]. Moreover, the amino acid which has been shown to play an important role in MPS is leucine [ 68 ]. Leucine supplementation can increase the rate of MPS in young adults [ 69 ] and can reduce the loss of lean mass in middle-aged adults (52 ± 1 years) during periods of bed rest [ 70 ]. According to PROT-AGE recommendations, 2.5–2.8 g of leucine per meal is sufficient to reach anabolic threshold and optimise MPS [ 3 ]. In general, plants contain a lower content of leucine (<8% of total protein) in comparison to animal-originated foods (approx. 8–14%), with maize being an exception (12%) [ 58 ]. However, some plants are still a relatively good source, if consumed in larger volumes and these include: dried seaweed (4.95 g/100 g), dry-roasted soy beans (3.22/100 g), roasted pumpkin seeds (2.39 g/100 g), dry-roasted peanuts (1.53 g/100 g), and cooked lentils (1.29 g/1 cup) [ 71 ]. As suggested by other authors, solutions to maximise essential amino-acids content of plant foods include: amino-acid complementation (consuming cereals and pulses in one meal), consuming higher amounts of plant-based products on a more frequent basis or enhancing the nutritional quality of crops through genetic engineering [ 44 , 58 , 72 ]. More studies are needed to evaluate the effectiveness of plant proteins in the prevention of muscle mass and strength loss. Sources other than soy and foods or diets that are complementary in terms of amino-acid composition (e.g., composed of more than one plant) have been poorly studied.

As concluded earlier, there is strong evidence that for optimal MPS and to prevent muscle loss an ageing adult would benefit from an increase (>1.2 g/kg/bw) in protein intake [ 3 , 11 ]. Ideally, proteins should be consumed three times a day with a dose of around 25–30 g of high-quality, yet sustainable protein in each meal [ 39 , 40 , 41 , 42 ]. However, the increased consumption of plant proteins found in whole foods (e.g., legumes, cereals, vegetables) stipulates more than one change in diet composition, i.e., apart from the increased percentage of energy yielded from proteins, dietary fibre—an integral element of all plant diets—can also be elevated considerably [ 82 ]. A diet high in both protein and fibre was demonstrated to support successful weight-loss [ 83 ]. Therefore, the incorporation of increased amounts of high-protein and high-fibre foods provides a promising strategy for overweight and obese individuals, since high-protein diets are linked to improved satiety and appetite control [ 84 ]. On the other hand, this also raises concerns about whether satiety will be enhanced by the two components, resulting in reduced appetite in individuals at risk of malnutrition. It is still unclear whether plant proteins affect appetite in the same way as animal proteins, and whether they compromise subsequent energy intake. However, it is worth emphasising that self-reported appetite is not necessarily a predictor of energy intake [ 85 ]. This section will briefly explain appetite-related mechanisms and will discuss the existing evidence regarding the potential effect of a diet high in plant proteins on appetite, across body mass index (BMI) categories. 4.1. Hunger, Satiety and Appetite Mechanisms It is important to stress that hunger and appetite are nonsynonymous terms. Hunger is defined as a physical ‘need to eat’ (usually caused by a long inter-meal interval), while appetite is a ‘desire to eat’ [ 86 ]. By contrast, satiation is a state of fullness, after hunger is suppressed [ 86 ]. Hunger and satiation are crucial elements of appetite assessment, which are usually scored using a visual-analogue scale [ 87 ]. Although a great deal of research has studied the phenomenon of appetite, underlying mechanisms remain unclear. In simple terms, hunger, satiation and appetite can be directly or indirectly stimulated by hormonal responses from: (i) pancreas, e.g., secretion of insulin, glucagon, pancreatic polypeptide (PP) and amylin; (ii) adipose tissue, e.g., leptin and adiponectin; (iii) gastrointestinal tract, e.g., ghrelin, glucagon-like peptide 1 and 2 (GLP-1, GLP-2), cholecystokinin (CKK), gastric inhibitory polypeptide (GIP), polypeptide YY (PYY), oxyntomodulin and serotonin; and iv) hypothalamus, e.g., dopamine, neuropeptide Y, growth hormone releasing peptide (GHRP) [ 88 , 89 ]. Some hormones or peptides promote appetite (orexigenic) and other work antagonistically, by suppressing it (anorexigenic) [ 88 , 89 ]. Apart from physiological factors, the sensorial exposure to food (e.g., sight, smell, taste) has been shown to increase appetite [ 90 ]. As such, people may report the desire to eat in the absence of hunger. A novel finding is that the individual’s protein status can affect the response to food cues. Griffoen-Roose and colleagues [ 91 ] discovered, that protein deprivation modulated reward responses in the brain and promoted a selective preference for savoury foods. Appetite control mechanisms have been suggested to be dependent on the individual’s body mass status and age [ 92 , 93 ]. The most consistent finding is that hunger and appetite tend to be reduced in older individuals (anorexia of ageing) [ 94 , 95 ]. Yet, it remains to be determined how the foods high in plant proteins influence physiological, sensorial and psychological responses, and whether they change with body weight status and age. Because of the sparsity of evidence, studies with younger participants have been included in the following section of this review.

Plant proteins (similarly to animal proteins) have been shown to induce fullness more effectively in normal weight subjects than in obese individuals, even when plant sources other than soy were tested. This can be explained by possible impairments in appetite control mechanisms observed among people with higher BMI [ 103 , 104 ]. An interesting study by Nilsson and others [ 105 ] investigated the effects of an evening meal composed of brown beans on appetite-regulating hormones in young adults (23.8 ± 0.7 years; BMI 22.5 ± 0.6 kg/m 2 ). They found a significant increase in PYY (by 51%) and decrease in ghrelin and hunger feeling (by 15 and 14%, respectively), when compared to the reference meal (white wheat bread). Although the observed responses were believed to be induced by the colonic fermentation caused by the starch found in brown beans, a protein-induced satiety response cannot be entirely ruled out. Several studies did not find significant differences between animal and plant proteins in terms of appetite control in normal weight adults. Lang and colleagues [ 106 ] compared satiating effects of egg albumin, casein, gelatin, soy, pea and wheat gluten protein among young, healthy men. No significant differences were found between protein source and satiety, subsequent energy intake and insulin secretion. The authors suggested that carbohydrate and fat content of experimental meals may have affected the observed responses. A year later, the same research group reported different effects of casein, gelatin and soy protein ingestion on glucose, insulin and glucagon kinetics [ 107 ]. No effects were reported in terms of protein source and 24 h energy intake and only a weak effect of protein type on satiety was shown. Similar findings were reported by Douglas and colleagues [ 108 ], who compared the effects of two high-protein meals (beef vs. soy) on appetite, satiety and food intake in young adults (mean age 21 ± 1 years; BMI 23.4 ± 0.6 kg/m 2 ). To account for potential confounders, two types of meals were compared: macronutrient and fibre-matched (24 g of either beef or soy protein), and size-matched (beef: 24 g protein/1 g fibre; soy: 14 g protein/5 g fibre). Under both conditions studied, fullness and postprandial PYY and GLP-1 plasma concentration increased as anticipated. However, no differences between meat and soy protein ingestion were observed and, importantly, no differences were observed in subsequent energy intake and the time when the next meal was requested [ 108 ]. In contrast, a recent study in young, normal weight men observed, that high protein plant meal (beans and peas) resulted in lower appetite, hunger and food consumption and higher fullness and appetite, when compared to meat-based meal (veal and pork) [ 109 ]. However, this finding is restricted to young adults only. In summary, results indicate that high-quality proteins, regardless of the source, have similar effect on appetite in normal weight adults and could be therefore be used interchangeably.

5.1. Consumer-Focused More research is needed to explore how to build consumer awareness about the importance of sufficient protein intake for healthy ageing. Currently, high-protein foods are mainly targeted to athletes and those who aim to lose weight. The market offer of real food solutions is still modest, with the majority of high-protein products being enriched with protein derived from dairy (e.g., whey, casein). The critical question is whether the increased intake of protein for muscle health will be in the future promoted among the general population of ageing adults. For example, will this message be supported by policy makers and national guidelines, in a similar manner to the salt and sugar reduction recommendations. Moreover, the current EU labelling regulations prevent indicating the potential health benefits of the high-protein product content (e.g., health claims). Hence, today’s consumers may lack the essential knowledge of the potential health benefits associated with high-protein product consumption. Furthermore, it would be interesting to learn more about consumer’s attitudes towards increasing the consumption of sustainably sourced proteins: (i) whether they are ready to make more environmentally friendly choices by replacing animal proteins with those from plants [ 115 ] and (ii) do they have the knowledge and cooking skills that allow for the incorporation of various plant proteins into their everyday diet? Perhaps, at the introductory phase, ready meals and snacks high in plant proteins would be a preferred consumer choice. While answering these questions it would be worthwhile to investigate potential acceptance and effectiveness of two routes: new product development (NPD) and product reformulation. The latter, could be achieved through a ‘health by stealth’ strategy which has been shown to be successful elsewhere, e.g., gradual reduction of salt in products aimed at children [ 116 ]. In the protein scenario, animal-based ingredients in commonly consumed products could be gradually and partially replaced with plant alternatives, giving the consumer time to adjust to new flavours, smells, and textures. Lastly, more evidence regarding age-, BMI- and sex-related differences in appetite responses to plant protein meals is needed. Most studies to date were conducted in young men or young mixed-sex samples [ 100 , 101 , 102 , 105 , 106 , 108 ] with no comparisons between sexes being drawn. It was previously reported, that hunger, satiety and appetite responses are different in women and men [ 117 ]. To our knowledge, no studies have yet investigated the effects of a high-protein plant diet on appetite, accounting for sex differences in adults from different age groups and with different nutritional status.

The currently recommended protein intake for ageing adults may not be sufficient for muscle mass and strength maintenance. To minimise the adverse health and environmental effects of excess animal protein consumption, incorporation of sustainably sourced plant proteins may be a promising strategy. Unfortunately, healthy and environmentally friendly food solutions are still in the conceptual phase and require more supportive research-based evidence. Although the evidence regarding the effects of plant proteins on appetite is scarce, available data points towards the positive effects of replacing animal proteins with plant-originated protein in normal weight as well as overweight/obese individuals. More studies are needed to understand the effect of these protein sources on satiety, in underweight adults.