Abstract
Background
A more sustainable diet with fewer animal-based products has a lower ecological impact but might lead to a lower protein quantity and quality. The extent to which shifting to more plant-based diets impacts the adequacy of protein intake in older adults needs to be studied.
Objectives
We simulated how a transition towards a more plant-based diet (flexitarian, pescetarian, vegetarian, or vegan) affects protein availability in the diets of older adults.
Setting
Community.
Participants
Data from the Dutch National Food Consumption Survey 2019–2021 of community-dwelling older adults (n = 607) was used
Measurements
Food consumption data was collected via two 24 -h dietary recalls per participant. Protein availability was expressed as total protein, digestible protein, and utilizable protein (based on digestibility corrected amino acid score) intake. The percentage below estimated average requirements (EAR) for utilizable protein was assessed using an adjusted EAR.
Results
Compared to the original diet (∼62% animal-based), utilizable protein intake decreased by about 5% in the flexitarian, pescetarian and vegetarian scenarios. In the vegan scenario, both total protein intake and utilizable protein were lower, leading to nearly 50% less utilizable protein compared to the original diet. In the original diet, the protein intake of 7.5% of men and 11.1% of women did not meet the EAR. This slightly increased in the flexitarian, pescetarian, and vegetarian scenarios. In the vegan scenario, 83.3% (both genders) had a protein intake below EAR.
Conclusions
Replacing animal-based protein sources with plant-based food products in older adults reduces both protein quantity and quality, albeit minimally in non-vegan plant-rich diets. In a vegan scenario, the risk of an inadequate protein intake is imminent.
Keywords: Protein quality, Protein intake, Simulation study, PDCAAS, Sustainability, Amino acid composition
1. Introduction
The current food system largely contributes to adverse environmental changes, mainly through the high usage of water and land, as well as the emission of greenhouse gases [1]. Meat and dairy, the main protein sources in an omnivorous diet, contribute the most to the food-related ecological footprint. A transition to a more sustainable diet-one that contains more plant-based products and less meat, could increase food availability while releasing the burden on the environment [2]. Furthermore, research suggests that a higher adherence to sustainable diets could lower the morbidity of chronic diseases, including cardiovascular diseases, type 2 diabetes, and certain cancers [3]. Currently, the mean ratio between animal-based/plant-based protein in the diets of Dutch inhabitants (1–79 years) is 57/43% [4], while it is advised to increase these values to 40/60% [5].
When transitioning to a more sustainable diet, special attention should be given to dietary protein needs. Plant-based proteins are generally lower in protein quantity and quality, the latter because of poor digestibility and amino acid composition [6,7]. Protein quality is an important factor in determining how much of the ingested protein is utilizable by the body. The quality of a protein source is determined by the digestibility and proportion of indispensable amino acids (IAA) combined, known as the Protein Digestibility–Corrected Amino Acid Score (PDCAAS) [8].
For older adults, consuming sufficient protein is of great importance as it prevents them from, among others, losing muscle mass [9]. When transitioning to a more sustainable diet, they might become at risk for an inadequate protein intake if either protein quantity or quality is insufficient. Because older adults often suffer from early satiation and have a lower appetite in general; the lower protein quantity, quality and higher fibre content in plant-based products pose challenges to reaching a sufficient intake of high-quality protein [10].
Currently, it remains uncertain whether older adults can meet their protein requirements through a more sustainable diet. A previous study among the general Dutch adult population (age 18–79) showed that sufficient protein intake is feasible when shifting from a 40% towards a 60% plant-based protein scenario [11]. Another simulation study performed on data from the Dutch National Food Consumption Survey (DNFCS) (2007–2010) in a younger adult population (18–65 years) showed a decrease in protein intake of about 20% in a “no meat, no dairy” dietary pattern. Nevertheless, nearly no one fell below the Estimated Average Requirements (EAR). Notably, protein quality and digestibility were not incorporated in these analyses and the analyses were restricted to adults aged under 65.
In this manuscript, we present the results of a simulation study on the diets of older adults (age ≥65 years) and evaluate the impact of the transition to a more sustainable eating pattern on protein quantity and quality. We explored various scenarios, including, flexitarian, pescetarian, vegetarian, and vegan dietary patterns to calculate quantity and quality of protein intake based on amino acid score and digestibility.
2. Methods
2.1. Study design
Data from the Dutch National Food Consumption Survey (DNFCS 2019–2021) was used [12]. The DNFCS is a periodical, cross-sectional food consumption survey, conducted by the National Institute for Public Health and The Environment (RIVM) [12]. Recruitment was done by a market research agency (Kantar) and the survey population was designed to be a representative sample of Dutch inhabitants. In 4-weekly waves, invitations were sent to nationally representative stratified random samples based on the following sociodemographic factors: age, gender, region, degree of urbanization and education level. In each wave, the composition and size of the sample were adjusted based on the response obtained in the previous waves. In total, 9.701 people were invited to participate of whom 3.570 (response rate 36.8%) individuals aged 1–79 were included in the DNFCS 2019 – 2021. In the population aged 65–79, 1701 people were invited, 607 of whom were included [12]. For this study, only that group was used. Besides food consumption, self-reported data on age, sex, height, weight, level of education and employment, and lifestyle characteristics were collected.
The Utrecht University Medical Ethical Review Committee evaluated the study and concluded it was not subject to the Medical Research Involving Human Subjects Act (WMO) of the Netherlands (reference number 19–145/C)
2.2. Dietary intake and amino acid composition
Food consumption data was collected via two non-consecutive 24-h dietary recalls per participant using the GloboDiet program [13]. Both recalls were performed within 2–6 weeks of each other. Participants aged 70 or older were asked to fill in a food diary on two specified days (days before the interview) which was only used as a memory aid for the 24-h recall. Participants aged between 65 and 70 were interviewed twice via telephone, while individuals aged 70 or older were interviewed once at home and once via telephone. Because of data collection during the COVID-19 pandemic, some were interviewed twice via telephone. Interviews were done in all seasons and on all days of the week. Food consumption was categorized by food consumption occasion (three meals and four in between moments) category by the participants.
Protein intake was calculated based on the amino acid dataset developed by Wageningen University and Research. This dataset is based on the Danish (Frida), American (USDA), English (McCance and Widdowson) and Japanese food composition tables and previously described by Heerschop et al. 2023 [14]. In this dataset, both amino acid content per food item and protein digestibility factors per food group (n = 27) are available.
As transitioning towards a more sustainable dietary pattern can influence both quantity (total protein content), as well as quality (digestibility and amino acid composition), we calculated protein intake/availability in three different ways: total protein intake (quantity), available protein intake after digestibility and utilizable protein intake based on the PDCAAS (quality).
Protein intake was derived by multiplying the consumed quantity by the total amino acid content of each food item and summing these overall food items. For the protein content after digestibility, we multiplied the total amino acid content of each food item by its specific digestibility factor.
We used amino acid content to calculate total protein intake. Not every amino acid contains the same amount of nitrogen and not all nitrogen in food items is bound in protein [15]. Thus, the standard conversion factor as applied in food composition databases (nitrogen from chemical analyses, multiplied by 6.25 (standard nitrogen content) or 6.38 (dairy products [16]) is too high for most food groups, leading to an overestimation of protein when applying the standard conversion factor [15].
Utilizable protein intake based on the PDCAAS was calculated per meal occasion, as optimal combinations of IAA can only be used if these IAAs are eaten within a limited time frame (i.e., one meal) [17,18]. Those IAAs that cannot be used will likely be directly oxidized [19]. We calculated the sum of amino acids after digestibility for each meal occasion (3 main meals and 4 in-between-meal moments). We then evaluated the similarity factor of the available IAAs in each meal to the WHO reference protein set by dividing the amino acid content per gram protein of the meal by the WHO reference protein values [20]. The similarity factor was determined by the most limiting amino acid. If there was no limiting amino acid during a meal, the similarity factor was maximized at 100%. The similarity factor was then multiplied by the total amount of amino acids after digestibility for that meal/snack moment. For daily utilizable protein intake, we calculated the sum of all separate meal/snack moments.
The Dutch food composition database (NEVO) [21] was used to assess the ratio of plant- vs. animal-based protein in the scenarios, as the amino acid database does not contain data on the source of protein.
2.3. Simulation of dietary scenarios
To assess the impact of a transition towards a more sustainable food pattern, different scenarios were created, representing two flexitarian (40%/80% of the meat replaced), one pescetarian (no meat, but fish and other animal-based products are included), one vegetarian (no meat and fish, but other animal-based products are included) and one vegan dietary scenario (no fish, meat, and animal-based products are included).
First, all products of the DNFCS were checked for the presence of values in the amino acid database; those without information (53 out of 1816 items) were replaced with comparable products by a dietitian (JWB) or nutritionist based on protein content and product similarity. For instance, boiled hare was replaced by boiled rabbit. Thereafter, all unique products used in the DNFCS were assessed to check if they met the criteria for the pescetarian, vegetarian or vegan dietary scenarios. Next, food products that did not fit into a scenario were classified by the same dietitian (JWB) and nutritionist into a food group and suitable alternatives were sought, based on the type of food (same food groups) and the context in which these products are eaten (see Table 1, Table 2). Replacement products were judged on adequacy and agreed upon by all co-authors (all of whom are either nutritionists or registered dietitians).
Table 1.
Vegetarian alternatives used for replacements shown per food group, with energy and protein content per 100 grams.
| Name | Protein/100 gram | kcal/100 gram | Name | Protein/100 gram | Kcal/100 gram |
|---|---|---|---|---|---|
| Meat or fish | Sandwich fillings based on meat or fish | ||||
| Chicken egg | 12.3 | 128 | Egg salad | 7.3 | 255 |
| Mozzarella cheese | 18.7 | 253 | Gouda cheese 48+ | 22.9 | 369 |
| Vegetarian hamburger | 17.7 | 192 | Peanut butter | 20.0 | 651 |
| Vegetarian schnitzel | 15.2 | 226 | Spread sweet average | 2.7 | 393 |
| Plant based burger beyond meat | 15.0 | 252 | Hummus | 7.7 | 322 |
| Vegetarian meatballs | 17.1 | 169 | Vegan luncheon | 8.2 | 156 |
| Vegetarian burger with cheese | 15.9 | 231 | Cheese salad | 9.0 | 422 |
| Vegetarian meatball | 16.9 | 243 | Cream cheese | 5.3 | 291 |
| Valess schnitzel | 12.3 | 188 | Chicken egg | 12.3 | 128 |
| Gouda cheese 48+ | 22.9 | 369 | Cheese 30+ | 31.9 | 306 |
| Vegetarian sausage | 13.3 | 259 | Cheese spread | 14.3 | 231 |
| Vegetarian burger | 11.0 | 210 | Chocolate sprinkles | 5.8 | 446 |
| Bread with meat | Soup | ||||
| Cheese pastry | 9.2 | 579 | Soup clear w vegetables and noodles | 0.7 | 17 |
| Baguette cheese-onion | 10 | 242 | Soup clear vegetables | 0.4 | 10 |
| Bread currant | 7.8 | 273 | Soup thickened vegetables | 0.7 | 36 |
| Roll white soft | 9.7 | 262 | Soup thickened no filling | 0.6 | 40 |
| Savoury snack | Minced meat | ||||
| Crisp potato | 6.3 | 538 | Lentils green/brown boiled | 21.0 | 306 |
| Cocktail snacks nibb-it | 3.3 | 482 | Quorn minced | 13.0 | 97 |
| Cassave crackers | 1.4 | 474 | Vegetarian minced meat | 24.3 | 124 |
| Falafel unprepared | 6.8 | 208 | Quorn pieces | 14.0 | 114 |
| Mincemeat beyond meat | 17.0 | 252 | |||
| Vegan mincemeat beans | 17.0 | 182 | |||
Note: protein and kcal are based on Dutch food composition table (NEVO)(21).
Table 2.
Vegan alternatives used for replacements shown per food group, with energy and protein content per 100 grams.
| Name | Protein/100 gram | kcal/100 gram | Name | Protein/100 gram | Kcal/100 gram |
|---|---|---|---|---|---|
| Meat, fish, Meat replacements based on dairy/egg, eggs (dinner), cheese (dinner) | Sandwich fillings based on meat, fish, cheese, eggs (breakfast and lunch) | ||||
| lentils green/brown boiled | 21 | 306 | Peanut butter | 20.0 | 651 |
| Plant based burger beyond meat | 17 | 252 | Luncheon meat quorn | 7.1 | 89 |
| Falafel | 6.8 | 208 | Hummus natural | 7.7 | 322 |
| Vegan bean burger | 16.0 | 191 | Vegan bacon | 5.5 | 140 |
| Sausage beyond meat | 17.0 | 233 | Vegan luncheon meat | 8.2 | 156 |
| Tahoe soya curd | 11.6 | 113 | Vegan grill sausage | 8.3 | 163 |
| Vegan chicken burger | 13.0 | 220 | Sesame paste tahin | 21.9 | 602 |
| Plant based chicken vivera | 15.0 | 166 | Melt me smoky cheese | 8.3 | 270 |
| Vegan chicken | 21.0 | 142 | Vegan bacon strips | 5.0 | 170 |
| Vegan swedish balls | 9.6 | 158 | Vegan chicken filet | 8.3 | 165 |
| Vegan vegetable burger | 11.0 | 116 | Vegan sausage | 7.0 | 244 |
| Plant based chicken tenders | 15.0 | 202 | Spread sweet averaged | 2.7 | 393 |
| Bread with dairy or meat | Drink with dairy | ||||
| Roll white soft | 9.7 | 262 | Tea | 0 | 0 |
| Bread currant | 7.8 | 273 | Coffee | 0 | 0 |
| Bread brown/wholemeal | 10.5 | 235 | Drink soya original alpro | 3 | 39 |
| Bread rye dark | 5.6 | 193 | Water | 0 | 0 |
| Yoghurt, cream sweet, custard, pudding, desserts, ice cream | Minced meat | ||||
| Plant based alternative quark | 2.7 | 119 | Lentils green/brown boiled | 21.0 | 306 |
| Plant based alternative quark soya | 5.7 | 54 | Quorn minced | 13.0 | 97 |
| Yoghurt soybased fruit | 3.7 | 134 | Vegetarian minced meat | 24.3 | 124 |
| Havergurt greek style | 3.3 | 145 | Quorn pieces | 14.0 | 114 |
| Yoghurt soybased | 4.0 | 47 | Mincemeat beyond meat | 17.0 | 252 |
| Havergurt blue berry | 1.3 | 101 | Vegan mincemeat beans | 17.0 | 182 |
| Drink soya original alpro | 3.0 | 39 | Savoury snack | ||
| Original plant-based not milk | 2.2 | 34 | Crisp potato | 6.3 | 538 |
| Yoghurt soybased vanilla | 3.7 | 134 | Cocktail snacks nibb-it | 3.3 | 482 |
| Dessert soya alpro | 3.1 | 85 | Cassava crackers | 1.4 | 474 |
| Vly unsweated | 2.5 | 34 | Falafel unprepared | 6.8 | 208 |
| Ice cream coconutmilk | 1.2 | 85 | Sweet snacks | ||
| Soup | Turkish delight | 0 | 370 | ||
| Soup clear w vegetables and noodles | 0.7 | 17 | Popcorn sweet, popped wo oil | 9.9 | 389 |
| Soup clear vegetables | 0.4 | 10 | Chocolate dark w hazelnuts | 9.0 | 565 |
| Soup thickened vegetables | 0.7 | 36 | Wafer galette | 6.9 | 480 |
| Soup thickened no filling | 0.6 | 40 | Cream | ||
| Cream based on veg oil alpro cuisine | 2 | 166 | |||
| Cream based on veg oil Alpro Cuisine Light | 2 | 63 | |||
Note: protein and kcal are based on Dutch food composition table (NEVO)(21).
In the vegan scenario, obvious animal-based products – cheese, milk, eggs – were marked as unfitting in the diet. Products that possibly include animal-based ingredients, such as cake and chocolate sprinkles were left unchanged, as they have minimal impact on daily protein intakes. For each of the products that needed to be replaced in one or more dietary scenarios, a dietitian selected up to 12 different alternatives from the same food group. If information about the IAA content of less than 12 suitable replacements was available, fewer replacements were used for that food group. Replacements with comparable products were done in gram-for-gram substitution.
Each food product to be replaced was randomly replaced by one of the available alternatives using a random number generator. The flexitarian diets (flexitarian-40 and flexitarian-80) were simulated in two steps: first, 40% or 80% of all meat and fish products were randomly selected for replacement. Thereafter, the random number generator was used to replace those items with alternatives.
Table 1 shows the vegetarian alternatives, which were used in the pescetarian, flexitarian and vegetarian diets for each food group. Table 2 shows the vegan alternatives.
2.4. Data analysis
All analyses (simulations and protein/amino acid calculations) were performed with R version 4.2.3. Characteristics of included participants of the DNFCS were described using descriptive statistics. Continuous variables are presented either as mean and standard deviation (SD) or as median and interquartile range (IQR) while categorical variables are given in frequencies and percentages.
The habitual intake (total protein intake, available protein after digestibility utilizable protein intake) for each scenario was calculated using the Statistical Program to Assess Dietary Exposure (SPADE) [22]. Weighting factors (sociodemographic factors, week/weekend days, season) were used to make data nationally and seasonally representative. A one-part model for daily intakes was used, and results are shown as median intake (p50) with IQR (p25-p75). Graphs were made by using Graphpad 10.2.3.
For traditional calculations of adequate protein intake, an Estimated Average Requirement (EAR) of 0.66 gram of high-quality protein per kilogram of body weight per day (g/kg bw/day) is used. This is based on nitrogen balance studies that do not consider digestibility [23]. Even high-quality protein sources like meat and dairy can result in some protein loss due to digestibility (digestibility factor 0.90−0.95) [7]. Since the EAR does not incorporate digestibility and amino acid composition, it is unsuitable for evaluating utilizable protein intake based on PDCAAS. In addition, the EAR is not applicable for total intake in situations where quality is lower [23], as in our more plant-based scenarios.
As there is no guideline to assess the EAR based on the PDCAAS, we recalculated the standard EAR of 0.66 g/kg bw/day. We assessed which percentage of protein intake is lost due to protein quality. To do this, we used the original diet assuming that the quality in our data is comparable to the original nitrogen balance studies [23]. The median loss between total protein intake and utilizable protein intake based on PDCAAS in the original diet, 11.9% (IQR: 9.6–14.9%), was subtracted from 0.66 g/kg bw/day, resulting in an adjusted EAR of 0.58 g/kg bw/day as the reference value to estimate the prevalence of the population with adequate PDCAAS intake.
3. Results
In total, 607 participants were included, half of them being men. The median age was slightly higher in men (71 years) compared to women (69 years), and BMI was around 27 kg/m2 in both groups (Table 3). Men were more frequently highly educated (41% high) than women (27% high).
Table 3.
Characteristics of the participants and five more sustainable scenarios from the Dutch National Food Consumption Survey 2019-2021 aged 65 or higher stratified by sex.
| Characteristic | Men n = 311 (51%) | Women n = 296 (49%) |
|---|---|---|
| Age (Years) | 71 (68–84) | 69 (67–73) |
| BMI (kg/m2) | 26.9 (±4.5) | 26.8 (±5.4) |
| Education level (n; %) | ||
| Low | 96 (31%) | 132 (45%) |
| Middle | 89 (29%) | 83 (28%) |
| High | 126 (41%) | 81 (27%) |
| Number of food replacements | ||
| Flexitarian-40 | 771 | 596 |
| Flexitarian-80 | 1405 | 1010 |
| Pescetarian | 1355 | 901 |
| Vegetarian | 1709 | 1227 |
| Vegan | 4754 | 4058 |
| Percentage plant-based protein of total protein | ||
| Original diet | 39.0% | 37.7% |
| Flexitarian-40 | 43.7% | 42.6% |
| Flexitarian-80 | 52.2% | 49.7% |
| Pescetarian | 54.3% | 51.9% |
| Vegetarian | 59.1% | 54.2% |
| Vegan | 99.3% | 99.3% |
| Kcal intake | ||
| Original diet | 2188 (1947–2455) | 1741 (1539–1956) |
| Flexitarian-40 | 2220 (1982–2481) | 1761 (1560–1973) |
| Flexitarian-80 | 2252 (1998–2532) | 1791 (1583–2011) |
| Pescetarian | 2258 (2009–2538) | 1786 (1581–2002) |
| Vegetarian | 2278 (2023–2561) | 1799 (1591–2018) |
| Vegan | 2161 (1918–2429) | 1726 (1530–1932) |
Data is shown as number (%), median (IQR) or mean (SD). Note that the vegan scenario did not lead to 100% plant-based protein as products with a low amount of animal protein, such as cakes, were not replaced.
The lowest frequency of a food replacement was needed in the flexitarian-40 scenario (1367 times), while the highest frequency was needed to create the vegan scenario (8812 replacements). In the reference scenario, the plant-based proportion of total protein intake was 39.0% in men and 37.7% in women. In the vegetarian scenario, the plant proportion of total protein intake was 59.1% in men and 54.2% in women, while in the vegan scenario, plant-based protein was nearly 100%. Total energy intake remained relatively stable (Δ <100 kcal) for all scenarios in both genders.
The median habitual daily protein intake in the original diet was 82.5 grams (0.96 grams/kg bw/day) for men and 67.9 grams (0.94 grams/kg bw/day) for women (see Fig. 1A and B). Compared to the original diet, the difference in daily protein intake was relatively low in most scenarios (3–7 %) except in the vegan scenario where loss amounted up to 35% (53.6 grams for men and 44.1 grams for women).
Fig. 1.
Daily median protein intake, protein intake after correction for digestibility and utilizable protein intake of older adults (≥65 year) in the Dutch National Food Consumption Survey, stratified by gender and scenario.
Loss of protein due to digestibility was comparable for most scenarios (about 10%), but slightly higher in the vegan scenario (14%). In the flexitarian-40/80 pescetarian and vegetarian scenarios, utilizable protein intake was comparable with intake based on digestible protein. However, in the vegan scenario, utilizable protein intake was approximately 15% lower than intake based on digestible protein.
Compared to the original diet, utilizable protein intake in the vegetarian scenario differed by about 7 grams in men and 5 grams in women, whereas in the vegan scenario, this difference was about 28 grams (both genders).
In the original diet, the median utilizable protein intake per kg bodyweight per day was 0.85 in men and 0.82 in women (Fig. 1C and D). This was lower for each scenario with higher ratios of plant-based protein and was 0.78 (men) respectively 0.77 (women) in the vegetarian scenario. However, a large difference was seen in the vegan scenario where the utilizable protein intake was 0.45 g/kg bw/day (both genders).
In the reference scenario, the prevalence of intake below EAR (utilizable protein intake below 0.58 g/kg bw/day) was 7.5% in men and 11.1% in women. This was to 13.7% and 17.7% in the vegetarian scenario while in the vegan scenario, over 80% of older adults had an intake below EAR (both genders 83.3%).
Fig. 2 depicts protein intake and availability per meal moment. The median quantity of protein intake at breakfast was, depending on the scenario, approximately 10−13 grams of protein for men and 8−11 grams for women (Fig. 2A and B). Differences between scenarios were small. At breakfast, the proportion of protein that cannot be utilized due to digestibility or amino acid composition was 20% in most scenarios, but over 30% in the vegan scenario.
Fig. 2.
Median protein intake, protein intake after correction for digestibility and utilizable protein intake of older adults (≥65 year) in the Dutch National Food Consumption Survey, stratified by gender, eating occasion and scenario.
For lunch, intake in the original diet, flexitarian-40, flexitarian-80, pescetarian and vegetarian scenario was relatively comparable with approximately 22 grams of protein for men and 18 for women (Fig. 2C and D). In the vegan scenario, this was 15 and 12 grams. At lunch, the proportion of protein that cannot be utilized due to digestibility or amino acid composition was in the original diet, flexitarian-40, flexitarian-80, pescetarian and vegetarian scenario smaller than at breakfast (10−13%) but in the vegan scenario, this loss due to quality was again over 30%.
The highest median protein intake was observed at dinner (Fig. 2E and F). In agreement with breakfast and lunch, differences in intake between most scenarios (except vegan) were small and men consumed 31−35 grams and women, 24−28 grams. Again, the lowest intake was seen in the vegan scenario with 20 grams for men and 16 grams for women. At dinner, the proportion of protein that cannot be utilized due to digestibility or amino acid composition was 10−13% in most scenarios and 23% in the vegan scenario.
4. Discussion
This study aimed to assess how protein quantity and quality differ between the present dietary intake and various more plant-based eating patterns in Dutch older adults aged between 65 and 79. In our simulated diets, protein quality and quantity decreased with increasing proportions of plant-based protein. However, in all non-vegan scenarios, protein quantity and quality did not show large reductions. The vegan diet however led to severely lower protein quantity, especially when correcting for protein quality, leading to large proportions of older consumers not meeting the protein requirements.
The strong decrease in the vegan scenario was expected because of the low quantity and quality of plant-based products [6,7]. Only one previous study (French general population, 18–65 years n = 1678) simulated a full vegan pattern while incorporating protein quality [24]. This study adopted a more theoretical approach by substituting animal-based protein with plant-based protein without replacing specific products. It reported a decrease in utilizable protein intake, but the percentage of the population falling below the EAR was small, suggesting that a shift towards a vegan pattern is safe [24]. However, in their original diet, protein intake was much higher (∼1.30 g/kg bw/day) compared to what was observed in our study (∼0.85 g/kg bw/day).
A previous “no meat and no dairy diet” simulation study (eggs and fish were still allowed) performed on the DNFCS 2007–2010 led to a reduction of 20% of protein intake [25], which was 35% in our vegan scenario. In this study “clear meat and dairy products” were replaced with mostly soy products, which are high in protein and high in quality while we used processed meat replacements mostly lower in protein quantity and quality. The previous study demonstrated that less protein loss is possible when high-protein products are chosen as replacements.
Previous cross-sectional studies of vegetarian and vegan eating patterns -mostly conducted in the general adult population (18–65 years)- showed little to no risks from switching towards a vegetarian or vegan dietary pattern [26]. Protein intake was usually lower in the vegan group, but as the general intake in these studies was high, the vegan protein intake remained above the required levels. This could be explained by the fact that people who follow a vegan diet today are relatively aware of their health and food intake [27]. In addition, most previous studies did not consider digestibility and amino acid composition, whereas we have shown that -in a predominantly plant-based diet- the additional loss due to lower quality is nearly as large as the loss due to lower quantity. Therefore, we expect that studies of high plant-based protein diets that only assess total intake without considering digestibility and amino acid composition are likely to overestimate protein availability.
To our knowledge, only one cross-sectional study from Denmark has assessed protein quality using amino acid composition. This study (n = 40, age 16–59 years) showed that more than half of the measured daily requirements for either total protein or amino acids were not met. In particular, those with a low energy intake were at risk of low intakes [28].
Our vegetarian scenario nearly reached the recommended level of 60% plant-based protein [5] without a significant decline in loss of utilizable protein intake. This implies that older adults can maintain an adequate protein intake while eating less meat/fish. This is in line with previously performed simulation studies [29]. Notably, protein intake in our vegetarian scenario was comparable to the flexitarian/pescetarian scenarios. In all these scenarios, loss due to digestibility and amino acid composition was low. This is in line with a previous study that showed that protein quality is only a factor of interest when plant-based protein is above 70%(24).
The loss in protein intake (quantity) in all scenarios was mainly observed at dinner. This was expected as most protein during that meal moment comes from meat [30], which we replaced with alternatives that sometimes had lower protein quantities. The loss in protein quality was greatest at breakfast and lunch. During these meal occasions, 50–60 % of protein comes from plant-based products [30], mostly bread, short in lysine. In the original diet, animal-based products compensate for the lower quality. This compensation mechanism ceases when we replace animal products with plant-based ones that have much lower protein quality. To compensate for the low lysine content of one slice of bread (35 grams) one would need to combine it with, for example, 155 grams of hummus (beans, relatively rich in lysine) or one glass (200 ml) of soy milk.
Traditional calculations of protein, based on the Dutch food composition table [31], showed a median protein intake of 84.1 g/day for men and 73.1 g/day for women. In our calculations, based on an amino acid database, this was slightly lower, with 82.5 g/day and 67.9 respectively. As described in the methods section, this could be because of different methodologies of assessing the protein/amino acid content of products. However, it remains unclear why this difference was larger in women than in men.
Our study represents the first comprehensive assessment of protein availability specifically focused on older adults. As we used a nationally representative and relatively large dataset, our study provides a good overview of how the protein intake of older adults may be affected by a transition towards a more sustainable diet. The main strength of our study is the assessment of protein availability by incorporating both digestibility and amino acid composition. While most previous studies have focused solely on quantity [29], we highlight that, particularly in the vegan scenario, the adjustments for digestibility and quality are of equal importance. Another strength is the replacement strategy that we used. We opted for a realistic scenario in which (up to 12) realistic replacements within different food categories were selected by a dietitian and nutritionist.
However, the choice of replacements is also a limitation because a simulation study may not always adequately reflect real-life practice: original food products are often not replaced with alternatives of the same weight as products differ in volume and have a different impact on satiation and satiety. Especially in the vegan scenario, high-fibre products are expected to lead to earlier satiation and thus to the intake of smaller volumes of products eaten. Furthermore, we chose scenarios with meat replacements that are processed and convenient in preparation. Higher protein quality per meal in the vegan scenario is possible when smart combinations are made by also replacing other meal components, real-life practice shows that people usually replace an animal-based product with a similar plant-based alternative, without making other changes within the same meal [32]. Finally, we used a very strict timeframe to assess protein quality (within one meal moment). Although it is assumed that protein should be eaten within a limited time frame [17,18] it is unclear exactly how long this period should be. Our timeframe might be too tight, leading to an underestimation of protein availability, especially in the vegan scenario. However, as mentioned before, lysine shortage especially at breakfast and lunch is so large that even daily, this is not likely to be fully compensated by other products [24].
Another consideration that needs to be made is the consequence of lower protein intake in older adults, for example on bone and muscle health, [33]. Will this impair protein synthesis and lead to muscle loss [34]? Our study only focussed on protein intake without assessing other outcomes on, for instance, micronutrient intake and sustainability. Whether micronutrient requirements can be met in more plant-based eating patterns needs further study [5]. We expect that the scenarios we simulated are more sustainable as they contain less animal-based protein, but we performed no lifecycle assessments as this was not within the scope of our research. Future studies should focus on these aspects. Finally, this field of research is progressing rapidly. The reliability and validity of working with PDCAAS need to be further established [35].
To conclude: we showed in this simulation study that replacing animal-based with plant-based protein sources in the diet of older adults led to reductions in protein quantity and quality only when all animal-based foods were eliminated. Shifting to a flexitarian, pescetarian or vegetarian diet only marginally influenced protein intake and did not place older adults at risk for an inadequate protein intake. Changing protein intake to 60% plant-based protein seems to be safe for older adults in terms of protein intake. In contrast, a vegan pattern was associated with a substantial decline in protein availability, leading to a majority of older adults not reaching the recommended protein levels.
Funding
This research was partly funded by the Taskforce for Applied Research (grant number: RAAK.MKB16.012), part of the Netherlands Organization for Scientific Research (NOW), financed by the Dutch Ministry of Education, Culture and ScienceAND by a fund of the Dutch Dairy Association.
Funders had no role in the design, analyses and writing or the decision to submit the manuscript.
Data availability
Data described in the manuscript, code book, and analytic code will be made available upon request pending [e.g., application and approval, payment, other]
Author disclosures
None.
Conflict of interests
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
Thanks to Natasha Nalucha Mwala for checking on grammar and spelling.
AR, MdvdS designed research; JWB conducted research; JWB analyzed data; and JWB, PG, JL, AR, MO, MdvdS wrote the paper. MdvdS had primary responsibility for the final content. All authors read and approved the final manuscript.
Contributor Information
Jos W. Borkent, Email: jos.borkent@han.nl.
Pol Grootswagers, Email: pol.grootswagers@wur.nl.
Joost Linschooten, Email: j.linschooten@has.nl.
Annet J.C. Roodenburg, Email: a.roodenburg@has.nl.
Marga Ocké, Email: marga.ocke@rivm.nl.
Marian A.E. de van der Schueren, Email: marian.devanderschueren@han.nl.
References
- 1.González-García S., Esteve-Llorens X., Moreira M.T., Feijoo G. Carbon footprint and nutritional quality of different human dietary choices. Sci Total Environ. 2018;644:77–94. doi: 10.1016/j.scitotenv.2018.06.339. [DOI] [PubMed] [Google Scholar]
- 2.Chen C., Chaudhary A., Mathys A. Dietary change scenarios and implications for environmental, nutrition, human health and economic dimensions of food sustainability. Nutrients. 2019;11(4):856. doi: 10.3390/nu11040856. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3.Rocha J.P., Laster J., Parag B., Shah N.U. Multiple health benefits and minimal risks associated with vegetarian diets. Curr Nutr Rep. 2019;8(4):374–381. doi: 10.1007/s13668-019-00298-w. [DOI] [PubMed] [Google Scholar]
- 4.RIVM. Inname van eiwit, energie en microvoedingsstoffen ten behoeve van Gezondheidsraadadvies eiwittransitie. Resultaten van VCP 2029-2021 [Internet]. Bilthoven; 2023. Available from: https://www.wateetnederland.nl/sites/default/files/2023-12/2023-01 Memo inname van eiwit%2C energie en microvoedingsstoffen voor GR advies eiwittransitie_1.pdf.
- 5.Dutch health counsil. Advies gezonde eiwittransitie [Internet]. Den Haag; 2023. Available from: https://www.gezondheidsraad.nl/onderwerpen/voeding/documenten/adviezen/2023/12/13/advies-gezonde-eiwittransitie.
- 6.Herreman L., Nommensen P., Pennings B., Laus M.C. Comprehensive overview of the quality of plant- and animal-sourced proteins based on the digestible indispensable amino acid score. Food Sci Nutr. 2020;8(10):5379–5391. doi: 10.1002/fsn3.1809. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Hohnstein J. 2022. Protein digestibility [Internet] [cited 2024 Jan 23]. Available from: https://esharesearch.atlassian.net/wiki/spaces/GENFOOD/pages/738820126/Protein+Digestibility. [Google Scholar]
- 8.Leser S. The 2013 FAO report on dietary protein quality evaluation in human nutrition: recommendations and implications. Nutr Bull. 2013;38(4) [Google Scholar]
- 9.Bauer J., Biolo G., Cederholm T., Cesari M., Cruz-Jentoft A.J., Morley J.E., et al. Evidence-based recommendations for optimal dietary protein intake in older people: a position paper from the prot-age study group. J Am Med Dir Assoc. 2013;14(8):542–559. doi: 10.1016/j.jamda.2013.05.021. [DOI] [PubMed] [Google Scholar]
- 10.Lochlainn M.N., Cox N.J., Wilson T., Hayhoe R.P.G., Ramsay S.E., Granic A., et al. Nutrition and frailty: opportunities for prevention and treatment. Nutrients. 2021;13(7):2349. doi: 10.3390/nu13072349. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11.Heerschop S., van’ t veer P., Biesbroek S., Kanellopoulos A. Wageningen University; Wageningen: 2023. Het effect van een gemodelleerde verschuiving van een inname van 40% naar 60% plantaardig eiwit op de gezondheid van het voedingspatroon. [Google Scholar]
- 12.van Rossum C., Sanderman-Nawijn E., Brants H., Dinnissen C., Jansen-Van der Vliet M., Beukers M., et al. RIVM; 2023. The diet of the Dutch. Results of the Dutch National Food Consumption Survey 2019-2021 on Food Consumption and evaluation with dietary guidelines [Internet] Available from: https://www.rivm.nl/publicaties/diet-of-dutch-results-of-dutch-national-food-consumption-survey-2019-2021-on-food. [Google Scholar]
- 13.Slimani N., Casagrande C., Nicolas G., Freisling H., Huybrechts I., Ocké M.C., et al. The standardized computerized 24-h dietary recall method EPIC-Soft adapted for pan-European dietary monitoring. Eur J Clin Nutr. 2011;65(1):s5–15. doi: 10.1038/ejcn.2011.83. [DOI] [PubMed] [Google Scholar]
- 14.Heerschop S.N., Kanellopoulos A., Biesbroek S., et al. Shifting towards optimized healthy and sustainable Dutch diets: impact on protein quality. Eur J Nutr. 2023;62(5):2115–2128. doi: 10.1007/s00394-023-03135-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.Mariotti F., Tomé D., Mirand P.P. Converting nitrogen into protein - Beyond 6.25 and Jones’ factors. Crit Rev Food Sci Nutr. 2008;48(2):177–184. doi: 10.1080/10408390701279749. [DOI] [PubMed] [Google Scholar]
- 16.RIVM . RIVM; Bilthoven: 2023. NEVO-online 2023: background information [Internet] Available from: https://www.rivm.nl/sites/default/files/2023-11/NEVO-online_background_information_2023.pdf. [Google Scholar]
- 17.Boirie Y., Dangin M., Gachon P., Vasson M.P., Maubois J.L., Beaufrère B. Slow and fast dietary proteins differently modulate postprandial protein accretion. Proc Natl Acad Sci USA. 1997;94(26):14930–14935. doi: 10.1073/pnas.94.26.14930. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18.Phillips S.M., Chevalier S., Leidy H.J. Protein “requirements” beyond the RDA: implications for optimizing health. Appl Physiol Nutr Metab. 2016;41:565–572. doi: 10.1139/apnm-2015-0550. [DOI] [PubMed] [Google Scholar]
- 19.Adhikari S., Schop M., de Boer I.J.M., Huppertz T. Protein quality in perspective: a review of protein quality metrics and their applications. Nutrients. 2022;14:947. doi: 10.3390/nu14050947. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20.WHO . Report of a Joint WHO/FAO/UNU Expert Consultation [Internet] WHO Technical Report Series; 2007. Protein and amino acid requirements in human nutrition. Available from: https://iris.who.int/bitstream/handle/10665/43411/WHO_TRS_935_eng.pdf. [Google Scholar]
- 21.RIVM . RIVM; 2021. Dutch food composition table (NEVO-tabel 2021) [Google Scholar]
- 22.Dekkers A.L.M., Verkaik-Kloosterman J., van Rossum C.T.M., Ocké M.C. SPADE, a new statistical program to estimate habitual dietary intake from multiple food sources and dietary supplements. J Nutr. 2014;144(12):2083–2091. doi: 10.3945/jn.114.191288. [DOI] [PubMed] [Google Scholar]
- 23.Rand W.M., Pellett P.L., Young V.R. Meta-analysis of nitrogen balance studies for estimating protein requirements in healthy adults. Am J Clin Nutr. 2003;77(1):107–127. doi: 10.1093/ajcn/77.1.109. [DOI] [PubMed] [Google Scholar]
- 24.de Gavelle E., Huneau J.F., Bianchi C.M., Verger E.O., Mariotti F. Protein adequacy is primarily a matter of protein quantity, not quality: modeling an increase in plant: animal protein ratio in French adults. Nutrients. 2017;9(12):1333. doi: 10.3390/nu9121333. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25.Seves S.M., Verkaik-Kloosterman J., Biesbroek S., Temme E.H.M. Are more environmentally sustainable diets with less meat and dairy nutritionally adequate? Public Health Nutr. 2017;20(11):2050–2062. doi: 10.1017/S1368980017000763. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 26.Mariotti F., Gardner C.D. Dietary protein and amino acids in vegetarian diets—A review. Nutrients. 2019;11 doi: 10.3390/nu11112661. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 27.Hoffman S.R., Stallings S.F., Bessinger R.C., Brooks G.T. Differences between health and ethical vegetarians. Strength of conviction, nutrition knowledge, dietary restriction, and duration of adherence. Appetite. 2013:65. doi: 10.1016/j.appet.2013.02.009. [DOI] [PubMed] [Google Scholar]
- 28.Aaslyng M.D., Dam A.B., Petersen I.L., Christoffersen T. Protein content and amino acid composition in the diet of Danish vegans: a cross-sectional study. BMC Nutr. 2023;9(1) doi: 10.1186/s40795-023-00793-y. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 29.Soh B.X.P., Smith N.W., von Hurst P., McNabb W.C. Evaluation of protein adequacy from plant-based dietary scenarios in simulation studies: a narrative review. J Nutr. 2024;154:300–313. doi: 10.1016/j.tjnut.2023.11.018. [DOI] [PubMed] [Google Scholar]
- 30.RIVM . RIVM; 2023. DNFCS 2019-2021: Mean contribution (%) of a moment to nutrient intake [Internet] Available from: https://statline.rivm.nl/#/RIVM/nl/dataset/50123NED/table. [Google Scholar]
- 31.RIVM. DNFCS 2019-2021:Habitual intake of nutrients from foods only [Internet]. [cited 2024 Jan 23]. Available from: https://data.overheid.nl/dataset/43483-dnfcs-2019-2021-habitual-intake-of-nutrients-from-foods-only.
- 32.Gehring J., Touvier M., Baudry J., Julia C., Buscail C., Srour B., et al. Consumption of ultra-processed foods by pesco-vegetarians, vegetarians, and vegans: associations with duration and age at diet initiation. J Nutr. 2021;151(1) doi: 10.1093/jn/nxaa196. [DOI] [PubMed] [Google Scholar]
- 33.Groenendijk I., de Groot L., Tetens I., Grootswagers P. Discussion on protein recommendations for supporting muscle and bone health in older adults: a mini review. Front Nutr. 2024;11 doi: 10.3389/fnut.2024.1394916. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 34.Ewy M.W., Patel A., Abdelmagid M.G., Mohamed Elfadil O., Bonnes S.L., Salonen B.R., et al. Plant-based diet: is it as good as an animal-based diet when it comes to protein? Curr Nutr Rep. 2022;11 doi: 10.1007/s13668-022-00401-8. [DOI] [PubMed] [Google Scholar]
- 35.Marinangeli C.P.F., House J.D. Potential impact of the digestible indispensable amino acid score as a measure of protein quality on dietary regulations and health. Nutr Rev. 2017;75(8) doi: 10.1093/nutrit/nux025. [DOI] [PMC free article] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
Data described in the manuscript, code book, and analytic code will be made available upon request pending [e.g., application and approval, payment, other]


