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EDITED BY

RUI POÍNHOS



Faculty of Nutrition and Food Sciences, University of Porto, Portugal

REVIEWED BY

AMANDA G. SÁ



Federal University of Santa Catarina, Brazil

ANNE PIHLANTO



Natural Resources Institute Finland (Luke), Finland

TABLE OF CONTENTS

 * * Abstract
   * Introduction
   * Materials and methods
   * Results
   * Discussion
   * Preprint
   * Data availability statement
   * Author contributions
   * Funding
   * Acknowledgments
   * Conflict of interest
   * Publisher’s note
   * Supplementary material
   * Abbreviations
   * References


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ORIGINAL RESEARCH ARTICLE

Front. Nutr., 15 June 2023
Sec. Nutrition and Sustainable Diets
Volume 10 - 2023 | https://doi.org/10.3389/fnut.2023.1178121

THIS ARTICLE IS PART OF THE RESEARCH TOPIC

Plant-Based Diets for a Sustainable Future

View all 10 Articles


PLANT TO ANIMAL PROTEIN RATIO IN THE DIET: NUTRIENT ADEQUACY, LONG-TERM HEALTH
AND ENVIRONMENTAL PRESSURE

Hélène Fouillet1*, Alison Dussiot1, Elie Perraud1, Juhui Wang1, Jean-François
Huneau1, Emmanuelle Kesse-Guyot2 and François Mariotti1*
 * 1Université Paris-Saclay, AgroParisTech, INRAE, UMR PNCA, 91120, Palaiseau,
   France
 * 2Université Sorbonne Paris Nord and Université Paris Cité, Inserm, INRAE,
   CNAM, Center of Research in Epidemiology and StatisticS (CRESS), Nutritional
   Epidemiology Research Team (EREN), F-93017, Bobigny, France

Background: Animal and plant protein sources have contrasting relationships with
nutrient adequacy and long-term health, and their adequate ratio is highly
debated.

Objective: We aimed to explore how the percentage of plant protein in the diet
(%PP) relates to nutrient adequacy and long-term health but also to
environmental pressures, to determine the adequate and potentially optimal %PP
values.

Methods: Observed diets were extracted from the dietary intakes of French adults
(INCA3, n = 1,125). Using reference values for nutrients and disease burden
risks for foods, we modeled diets with graded %PP values that simultaneously
ensure nutrient adequacy, minimize long-term health risks and preserve at best
dietary habits. This multi-criteria diet optimization was conducted in a
hierarchical manner, giving priority to long-term health over diet proximity,
under the constraints of ensuring nutrient adequacy and food cultural
acceptability. We explored the tensions between objectives and identified the
most critical nutrients and influential constraints by sensitivity analysis.
Finally, environmental pressures related to the modeled diets were estimated
using the AGRIBALYSE database.

Results: We find that nutrient-adequate diets must fall within the ~15–80% %PP
range, a slightly wider range being nevertheless identifiable by waiving the
food acceptability constraints. Fully healthy diets, also achieving the
minimum-risk exposure levels for both unhealthy and healthy foods, must fall
within the 25–70% %PP range. All of these healthy diets were very distant from
current typical diet. Those with higher %PP had lower environmental impacts,
notably on climate change and land use, while being as far from current diet.

Conclusion: There is no single optimal %PP value when considering only nutrition
and health, but high %PP diets are more sustainable. For %PP > 80%, nutrient
fortification/supplementation and/or new foods are required.




INTRODUCTION

Historical and current nutritional transitions are coupled with changes in the
relative contribution of dietary animal and plant proteins. This has been
studied from hunter-gatherers to post-agricultural societies (1), from
traditional diets that enabled thriving civilizations to diets in
post-industrialized countries (2, 3), and more recently, in Western countries
with the emerging trend toward more plant-predominant diets.

Changes in plant and animal protein intake raise classic nutritional questions.
One in particular concerns the possible risk of some nutrient shortage with
diets too low in animal protein, since animal protein foods contribute
significantly to the intake of indispensable nutrients like iron, calcium and
vitamin B12, whose overt deficiencies have various adverse health consequences
(such as anemia and higher risk of osteopotosis) (4, 5). However, plant proteins
are also important for the intake of fiber and some indispensable nutrients
(like vitamins B9 and C), which modulate short and long-term disease risk, and
are also lower in saturated fats that are excessively consumed (6, 7). Beyond
the relationship to nutrient adequacy, animal/plant proteins and their packages
largely affect the metabolome and the microbiota and physiological functions
that are crucial for long-term health (6, 8–10). Accordingly, there have been
many contrasting associations reported recently between plant and animal protein
intake and mortality, especially regarding cardiovascular diseases (6, 11, 12).

More globally, plant (such as legumes, nuts and whole grains) and animal (such
as red and processed meats) protein sources have heterogeneous relationships to
nutrient adequacy (13) and to long-term health regarding cardiovascular diseases
(9, 14–16) and cancers (17, 18). There is indeed a challenge for food-based
dietary guidelines to point out what proportions of plant and animal protein
foods should be recommended (19, 20). However, the plant to animal protein ratio
remains a poor, summarizing descriptor of dietary patterns, since two diets with
the same plant to animal protein ratio can actually be very different (9). There
is thus a need to analyze the overall proportion of plant protein in the diet in
view of the related dietary profiles and their nutritional adequacy and
healthiness.

Furthermore, current interest in the proportions of plant and animal proteins in
the diet also stems from their differential association with environmental
pressures, in particular greenhouse gas emissions (GHGe) and land use (21–24).
Altogether, the plant to animal protein ratio in the diet appears central to the
sustainability of the food systems (21, 25). This has implications for dietary
guidelines that aim to encompass both human and planetary health (26–28).

Thus, the literature lacks an analysis of what proportion of plant protein in
the diet (%PP, the percentage of plant protein in total protein intake) is
adequate and, even further, what proportion is optimal from a unified nutrition
and health perspective that also considers the impact on other aspects of
sustainability. We hypothesized that %PP could be safely increased well beyond
its current low level, but will certainly be limited by a too-low level of
animal protein. We also hypothesized that, rather than an optimal value, there
may be a relatively wide range of %PP values that would be similarly adequate,
when considering only human nutrition and health. Here, using advanced diet
modeling and optimization, we studied whether an optimal %PP value can be
identified when taking into account the reference values for nutrients and the
disease burden risks for food categories. We characterized modeled diets that
departed as little as possible from prevailing diets at all levels of adequate
%PP values for nutrient adequacy and long-term health to identify nutritional
issues (i.e., limiting nutrients) and dietary levers (i.e., effective foods). We
furthermore estimated the environmental pressures associated with modeled diets
along the whole range of adequate %PP values.


MATERIALS AND METHODS


INPUT OF DIETARY DATA

The data used for this study were extracted from the French Individual and
National Study on Food Consumption Survey 3 (INCA3) conducted in 2014–2015. The
INCA3 survey is a representative cross-sectional survey of the French
population; its method and design have been fully described elsewhere (29).
Males aged 18–64 years (n = 564) and pre-menopausal females aged 18–54 years (n
= 561), not identified as under-reporters, were included in the present study;
the final sample contained 1,125 adults (Supplementary Figure S1).

Dietary data were collected by professional investigators assisted by a
standardized and validated dietary software (GloboDiet) from three unplanned,
non-consecutive, 24 h dietary recalls spread over a three-week period (two
weekdays and one weekend day). Portion sizes were estimated using validated
photographs (29), and the nutrient contents of different food items came from
the 2016 food composition database operated by the French Information Centre on
Food Quality (CIQUAL) (30). Mixed foods were broken down into ingredients and
then gathered into 45 food groups (Supplementary Table S1). For each sex, the
nutrient content of each food group was calculated as the mean nutrient content
of food items constituting the food group weighted by their mean intake by the
sex considered, as previously described (31). All dietary data (food group
consumption and nutrient content) relate to the total population of each sex
(including non-consumers).


MULTI-CRITERIA DIET OPTIMIZATION UNDER CONSTRAINTS

Using multi-criteria optimization, we identified modeled diets (i.e., modeled
consumptions of the 45 food groups) with a minimal long-term health risk and a
minimal departure from the observed diet (taking into account cultural
acceptability and inertia), under constraints that would ensure adequate
nutrient intakes and remain within current consumption limits. In this context,
we investigated the role of %PP to identify its adequate range of variations and
to characterize the dietary, nutritional and environmental consequences of these
variations.

This non-linear optimization problem was performed using the NLP solver of the
OPTMODEL procedure of SAS software version 9.4 (SAS Institute Inc., Cary, NC,
USA). Optimization was implemented at the population level but in males and
females, separately. The optimized diets of males and females were then averaged
to derive optimized diets for the adult population.


OBJECTIVES

The main optimization objective was to minimize the long-term health risk of the
modeled diet, as assessed by the Health Risk (HR) criterion. The HR criterion
was set to target the dietary recommendations from the Global Burden of Diseases
(GBD) based on epidemiological studies about the associations between
consumption of different food groups and risk of chronic diseases (32). The HR
criterion thus aimed to limit the consumption of three unhealthy food groups or
categories (red meat, processed meat and sweetened beverages), while promoting
that of six healthy food groups or categories (whole grain products, fruits,
vegetables, legumes, nuts and seeds, and milk) until their minimum risk exposure
levels (TMREL) were reached. According to the most recent (2019) estimates from
the GBD, TMREL values were 0 g/d for red meat, processed meat and sweetened
beverages, and 150, 325, 300, 95, 14.5 and 430 g/d, respectively, for whole
grain products, fruits, vegetables, legumes, nuts and seeds, and milk (32). In
our study, the HR criterion was thus expressed and minimized as:

minHR=∑3i=1(Opt(i)Max(i)×DALYs(i)DALYs(all))+∑6j=1(max[TMREL(j)−Opt(j)TMREL(j);0]×DALYs(j)DALYs(all))minHR=∑i=13OptiMaxi×DALYsiDALYsall+∑j=16maxTMRELj−OptjTMRELj0×DALYsjDALYsall


where i denotes the food groups to be decreased (red meat, processed meat and
sweetened beverages), j denotes the food groups to be increased (whole grain
products, fruits, vegetables, legumes, nuts and seeds, and milk), Opt(i) and
Opt(j) are the optimized consumptions of food groups i and j, respectively (in
g/d), Max(i) is the upper limit of consumption of food group i (in g/d),
TMREL(j) is the TMREL value of food group j (in g/d), DALYs(i) and DALYs(j) are
the disability-adjusted life-years (DALYs) associated with excessive or
insufficient consumptions of food groups i and j, respectively (in y), and
DALYs(all) is the sum of all DALYs(i) and DALYs(j). The Max values used were the
maximal recommended consumption of unhealthy foods in line with the French
dietary guidelines (33): 71 g/d for red meat, 25 g/d for processed meat and
263 g/d (corresponding to the average portion size) for sweetened beverages
intake. The TMREL and DALYs values used were issued from the most recent (2019)
estimates from the GBD (32) adapted to our study context (by using sex-specific
and French DALYs values, Supplementary Table S2).

We also evaluated how the modeled diets deviated from current diets, in order to
consider inertia to changes in food consumption, which is one way to account for
social/cultural acceptability. The Diet Departure (DD) criterion was defined as
the sum of the squares of the differences between observed and optimized food
group consumption, standardized by their observed standard deviations, as
previously explained (31). DD was thus expressed and minimized as:

minDD=∑nk=1[Obs(k)−Opt(k)SD(k)]2minDD=∑k=1nObsk−OptkSDk2


where k is the number of food groups (n = 45), Obs(k) and Opt(k) are,
respectively, the observed and optimized consumption of food group k (in g/d)
and SD(k) is the current standard deviation of the consumption of food group k.


CONSTRAINTS

During diet optimization, the total energy intake was constrained to stay within
±5% of its observed value. Thirty-five nutritional constraints were applied to
ensure adequate nutrient intake in the male and female populations
(Supplementary Table S3), based on the most recent reference values from the
French Agency for Food, Environmental and Occupational Health & Safety (ANSES)
(34). We did not consider any constraints for vitamin D, because its reference
value is known to be much too high to be reached by a non-fortified diet alone
(31, 33). As the absorption of iron and zinc is dependent on dietary factors,
the requirements were based on bioavailable iron and zinc calculated from the
dietary intake using equations that predict their absorption (35–37), as
detailed in a previous study by our group (31). This previous study had
demonstrated that current recommendations regarding bioavailable iron and zinc
are very constraining when trying to model healthier diets, these
recommendations being much higher than current intakes (e.g., there is a current
iron-deficiency anemia prevalence of 4.1% in French women) (31). Therefore, like
in this previous study, we used threshold values lower than current reference
values. They correspond to a deficiency prevalence of 5%, because such
flexibility enables the identification of diets that are apparently healthier
overall, with a better balance in DALYs due to less cardiometabolic disease,
despite a higher prevalence of iron-deficiency anemia (31). In addition, to take
into account the slightly lower digestibility of plant vs animal proteins
regarding the nutritional constraint on protein requirement, a 5% penalty was
applied to protein intake from plant protein food items, as previously described
(38). As the intake of individual amino acids is generally adequate when the
protein intake is sufficient in a varied diet (39), only protein requirements
were considered in the model constraints, but we have a posteriori verified that
modeled diets also contained adequate intakes of indispensable amino acids by
using a database of the amino acid composition of food groups (Supplementary
Information Text S1).

Moreover, some acceptability constraints were applied to the food group
consumption (Supplementary Table S4). Acceptability constraints aimed to keep
the food group intakes within the range of observed intakes, by bounding each
food group intake between its 5th and 95th percentile of observed consumption in
males and females separately. We did not do this for the unhealthy food groups
or categories (red meat, processed meat and sweetened beverages), for which a
dietary constraint with an upper limit was already defined according to the
French dietary guidelines. Another exception was made for some healthy food
groups (legumes and milk) that had 95th percentile values slightly lower than
TMREL values, and for which the upper limit has thus been raised to their TMREL
values.


OPTIMIZATION STRATEGY

We firstly aimed to determine the range of adequate %PP values in the diet that
would ensure nutrient adequacy with a minimal long-term health risk. This first
problem of identifying the adequate %PP range was addressed by optimizing the HR
criterion under all the nutritional and acceptability constraints, with an
additional constraint on %PP that was iteratively parameterized according to a
grid search. This grid search constraint forced the %PP value to be equal to x%,
with x% varying from 0 to 100% by steps of 5% (or even 1% at the edges of the
adequate %PP range). As this problem was often non-uniquely identifiable,
leading to different solutions with slightly distinct dietary patterns but
similar HR values (especially for the intermediate %PP values that allowed for a
variety of food group combinations with a similarly null HR value), we choose to
systematically select the dietary solution that was the most acceptable a
priori, based on the lowest departure from the current diet. According to the
hierarchical method in multi-criteria optimization (40), this second problem of
diet selection was addressed in a second stage. This time it was done by
optimizing the DD criterion under the constraint that HR was equal to its
previously identified minimal value, always under all the nutritional and
acceptability constraints, and the grid search constraint on %PP covering its
previously identified adequate range.


LIMITING NUTRIENTS AND CONTRIBUTION OF FOOD GROUPS TO THEIR INTAKE

We conducted a dual value analysis to better characterize the tensions between
%PP, nutrient adequacy and long-term health. We reported the dual values
associated with the %PP equality constraint and the nutritional constraints
during HR optimization (obtained during the first problem solving, as explained
above), which represent the potential HR gain if the limiting bound (lower or
upper) of the considered constraint was relaxed by one unit. In order to compare
the relative influence of nutrients, their dual values were standardized to
represent the potential HR gain if the limiting bound was relaxed by 10%, to
classify nutrients from the most limiting (higher absolute standardized dual
value) to the least limiting (lowest absolute standardized dual value).

For the most limiting nutrients in the different modeled diets (i.e., nutrients
with the most active constraints), we studied contributions of different food
groups to intake of that particular nutrient in each modeled diet identified for
each adequate %PP value (i.e., in the modeled diets resulting from the second
problem solving, as explained above).


SENSITIVITY ANALYSIS

We also conducted a sensitivity analysis to assess the influence of some
constraints of particular interest. We thus compared the results obtained when
requiring the deficiency prevalence to be ≤1% rather than ≤5% (main model) in
the nutritional constraints for bioavailable iron and zinc (their alternative
threshold values are given in Supplementary Table S3), and when removing or not
(main model) all the dietary and acceptability constraints on food group
intakes.


DIET ENVIRONMENTAL IMPACTS

Finally, to assess environmental pressures related to the observed and modeled
diets, we used the French agricultural life cycle inventory database AGRIBALYSE®
v3.1; its methodological approach (summarized in Supplementary Information Text
S2) has been described elsewhere (41–43). In particular, we evaluated the
food-related GHGe (in kg CO2eq, with the non-CO2 GHGe included and weighted
according to their relative impact on warming), land use (referring to the use
and transformation of land, dimensionless), water use (relating to the local
scarcity of water, in m3 water deprivation) and fossil resource use (use of
non-renewable fossil resources such as coal, oil, and gas, in MJ), together with
a single environmental footprint score (dimensionless) that aggregated 16
indicators (44).


RESULTS


RANGE OF ADEQUATE %PP VALUES AND IDENTIFIED TENSIONS BETWEEN %PP, NUTRIENT
ADEQUACY AND LONG-TERM HEALTH

The adequate %PP range compatible with nutrient adequacy was 16–82% in males and
16–77% in females, and only the 25–70% %PP range was additionally compatible
with a minimal health risk (HR criterion) for both sexes (Table 1). In this
narrower range, a null HR value was attained by the removal of unhealthy foods
(red meat, processed meat and sweetened beverages) and an increase in healthy
foods (whole grain products, fruits, vegetables, legumes, nuts and seeds, and
milk) up to or above their TMREL values (32).


TABLE 1

Table 1. Range of adequate values of the percentage of plant protein in the diet
(%PP) and corresponding minimal values of long-term health risk (HR criterion)
in French males and females.




Among the %PP equality constraint and the nutritional constraints, none were
found limiting for HR minimization over the 25–70% %PP range (Table 2). The %PP
equality constraint was limiting only for %PP values lower than 25% (strongly)
and higher than 70% (more moderately, due to the lower HR impact of the milk
decrease for the highest %PP values than of the red meat increase and whole
grain product decrease for the lowest %PP values). Nutrients identified as
increasingly limiting as %PP decreased below 25% were fiber, sugar (excluding
lactose), saturated fatty acids and atherogenic fatty acids (lauric, myristic
and palmitic acids). As %PP decreased below 25%, it was hence increasingly
challenging to maintain sufficient intake of fiber and non-excessive intakes of
sugar and fatty acids (as shown by the opposite sign of their dual values),
which resulted in dietary solutions of increasingly degraded HR values.
Nutrients that were identified as increasingly limiting when %PP increased above
70% were iodine, sodium, vitamin B2, calcium, EPA + DHA, vitamin A and
α-linolenic acid in both sexes together with vitamin B12 in males and
bioavailable iron in females. As %PP increased above 70%, it was increasingly
challenging to maintain sufficient intakes of these nutrients and a
non-excessive sodium intake. The other nutrients (n = 20, those not shown in
Table 2) were never limiting over the adequate %PP range, including, of note,
protein.


TABLE 2

Table 2. Dual values of the active constraints identified during minimization of
the long-term health risk (HR criterion) in French males and females1.




Sensitivity analysis showed that being more demanding for bioavailable iron and
zinc (i.e., constraining their deficiency prevalence at ≤1% rather than ≤5% as
in the main model) resulted in slightly restricting the adequate %PP range on
the right (16–79% in males and 16–70% in females), and the %PP range ensuring a
null HR value on both sides (30–65% in males and 35–45% in females) (data not
shown). Conversely, when suppressing all the food group consumption limits
(i.e., all the dietary and acceptability constraints) from the model
(Supplementary Table S5), the range of adequate %PP values was expanded on both
sides (8–94% in males and 8–92% in females), as was the %PP range ensuring a
null HR value (16–86% in males and 16–84% in females), but consistently with the
same limiting nutrients as in the main model (in particular, insufficient fiber
intake for excessively low %PP values, or insufficient intakes of vitamin B12,
iodine and EPA + DHA for excessively high %PP values).


MODELED DIETS

All the modeled diets identified (Figure 1; Supplementary Figure S2) were very
distant from the current typical French diets, with departure values (DD
criterion) equal to or greater than twice the standard deviation observed in the
population. Furthermore, most of the modeled diets with a null HR value (i.e.,
in the 25–70% %PP range) were all about equally distant from the observed diets,
with close DD values (differing by less than 20%) in the 35–65% %PP range and
similar DD values (differing by less than 5%) in the 45–60% %PP range.


FIGURE 1

Figure 1. Daily food category consumption in the observed diets (obs) and
modeled diets obtained by long-term health risk (HR) and diet departure (DD)
minimization under imposed percentage of plant protein in the diet (%PP) in
French adults. Results are reported for all the adequate %PP values ensuring
nutrient adequacy (16–77%), which includes those also ensuring a null HR value
(25–70%). The Bar charts represent the cumulative consumptions of food
categories (black axis on the left) and the curves represent the HR and DD
values (blue and pink axes on the right, respectively). For clarity, the 45
modeled food groups are not represented here but grouped into broader categories
that are included in HR (such as red and processed meats) or represent other
protein sources (such as poultry and seafood). Consumption of water, hot
beverages, alcohol and miscellaneous foods are not shown for clarity. Details
about food grouping and consumptions of food categories not shown here are given
in Supplementary Tables S1, S6, respectively.




Although the energy intake remained relatively stable between modeled and
observed diets (by construction), the total intakes of both animal-based and
plant-based foods were increased in the 25–70% %PP range, notably owing to the
important increases in milk, fruits and vegetables up to or above their TMREL
values (Supplementary Table S6; Supplementary Figure S3). Regarding plant
products, all the modeled diets exhibited dramatic increases in fruits and
vegetables, whole grain products and legumes and nuts. Regarding animal
products, red and processed meats were readily removed as %PP increased. These
meats were replaced by poultry and eggs, which transiently increased, the
modeled diets then being meat-free from PP% = 60%. Dairy and seafood were the
only remaining animal products at the right end of the adequate %PP range
(Supplementary Figure S3).

Over the entire adequate %PP range, including meat-free diets, the intakes of
protein and of each indispensable amino acid were always much higher than their
98% safe intake thresholds (Figure 2; Supplementary Table S7; Supplementary
Figure S4).


FIGURE 2

Figure 2. Contribution of food categories to protein intake in the observed
diets (obs) and modeled diets obtained by long-term health risk (HR) and diet
departure minimization under imposed percentage of plant protein in the diet
(%PP) in French adults. Results are reported for all the adequate %PP values
ensuring nutrient adequacy (16–77%), which includes those ensuring also a null
HR value (25–70%). Sections inside the bars represent the contributions of food
categories to protein intake (in g of protein/kg of BW/d). See Supplementary
Table S1 for the detailed composition of food categories.





CONTRIBUTIONS OF FOOD GROUPS TO LIMITING NUTRIENT INTAKES

Regardless of their %PP value, all the modeled diets were nutrient-adequate, in
contrast with observed diets (Supplementary Table S8).

As %PP increased, it was increasingly difficult to maintain sufficient intakes
of bioavailable iron, vitamins B12, B2 and A, and iodine and calcium, owing to
the decreases in the animal products that were their main contributors (red
meat, dairy products and eggs) (Supplementary Figure S5). The EPA + DHA and
α-linolenic acid intakes, which are largely insufficient in the observed diets,
were made sufficient in all the modeled diets by increases in their main
contributors, respectively, seafood and added fats, with difficulties to
maintain them sufficient for the highest %PP values (Supplementary Figure S5).
The sodium intake, which is dramatically excessive in the observed diets, was
reduced to its upper limit in all the modeled diets as a result of removing
processed meat and reducing refined grain products, with difficulties to
maintain sodium not excessive for the highest %PP values, due to increases in
some starch and miscellaneous foods (Supplementary Figure S5). Conversely, as
%PP decreased, it was increasingly difficult to maintain a sufficient intake of
fiber and non-excessive intakes of sugar and saturated fatty acids, due to the
meat and dairy increases (Supplementary Figure S6).


ENVIRONMENTAL IMPACTS OF MODELED DIETS

Across modeled diets, GHGe gradually decreased as %PP increased until %PP = 70%,
where the GHGe were ~ 50% lower than with the observed diet (Figure 3). Similar
trends were observed for land use and, to a lesser extent, fossil resource use
(Supplementary Figure S7), with 40% and ~ 20% decreases, respectively, from the
observed to the modeled diet with %PP = 70%. In contrast, water use was ~25–50%
higher for the null-HR modeled diets than for the observed diet, due to their
very high levels of fruits and vegetables that were by far the most
water-demanding food groups (Supplementary Figure S7). Overall, at the level of
the single environmental footprint score that aggregated 16 indicators, the same
trend was observed as for GHGe, with a 37% decrease in this aggregated score
from the observed to the modeled diet with %PP = 70% (Supplementary Figure S7).


FIGURE 3

Figure 3. Greenhouse gas emissions (GHGe) associated with the observed (obs) and
modeled diets obtained by long-term health risk (HR) and diet departure
minimization under imposed percentage of plant protein in the diet (%PP) in
French adults. Results are reported for all the adequate %PP values ensuring
nutrient adequacy (16–77%), which includes those ensuring also a null HR value
(25–70%). Sections inside the bars represent the contributions of food
categories to GHGe (in kg CO2-eq/d), and values above the bars represent the
relative deviation in GHGe from its observed value (in %). See Supplementary
Table S1 for the detailed composition of food categories.





DISCUSSION

Gathering all nutritional information over a large spectrum that covered
nutrient reference values and long-term health risks, our study formally
establishes ranges of plant protein proportion (%PP) for nutrient-adequate and
healthy diets. One major finding is that there is no optimal %PP value, as we
found a spectrum of similarly healthy diets over the 25–70% range. However,
diets in the upper end were associated with substantially lower GHGe and overall
environmental impact.

A wide dietary %PP range, from ~15 to 80%, was found compatible with providing
all nutrients in adequate amounts. Our results do not agree with those of Vieux
et al., who recently argued that %PP must be <50% to ensure nutritional adequacy
(45). However, in this diet optimization study, solutions with %PP >50% were
rejected not because of their true intrinsic inability to meet nutrient
requirements but because of an incorrect problem formulation, as we recently
pointed out (46). Furthermore, by not analyzing how the constraints considered
affected the results and by not identifying the limiting nutrients, this work
was not informative about the nutritional barriers to increasing %PP, which was
our concern here along with its other health and environmental impacts. In our
study, as shown by sensitivity analysis, the wide %PP range identified as
compatible with nutritional adequacy was slightly restrained by the considered
constraints for food acceptability, whereas the nutritional issues identified
remained broadly the same with or without these constraints. From a nutritional
viewpoint, no diet with %PP < ~15% was able to provide enough fiber and
non-excessive amounts of saturated fatty acids, while also satisfying all
constraints for nutrient intakes and food acceptability. In these too-low %PP
diets, inadequate fiber intake was due to insufficient consumption of whole
grains, legumes, and nuts, which were the most critical plant protein sources
with intakes below their minimum-risk exposure levels. More interestingly, given
the ongoing dietary transition, we could not find diets with %PP > ~80% that
would provide sufficient amounts of a large set of nutrients, particularly
iodine, vitamin B12 (in males), bioavailable iron (in females), calcium and
EPA + DHA. These nutrients are considered to be at issue in vegetarian diets
(except calcium and iodine in lacto-ovo-vegetarian), notably calcium and B12 in
predominantly plant-based diets (47, 48). From a dietary viewpoint, as shown
when approaching the critical value of %PP = 80%, dairy appeared to be key to
preventing iodine and calcium shortages. Seafood, meanwhile, appeared critical
to providing EPA + DHA (with oily fishes as the main source) as well as iodine
and B12. Milk and seafood were the last remaining animal products at the highest
%PP values, confirming their importance as healthy, nutrient-dense protein
sources (49). Healthy plant protein sources such as legumes and nuts apparently
could not replace milk or seafood. This is because they actually reached their
upper allowed intake very early (as soon as %PP = 25% for legumes), which
indicates that they constitute an effective dietary lever. However, even when
removing all food intake limits (in sensitivity analysis), it remained
impossible to obtain 100% plant-based diets because of the same nutritional
issues (insufficient intakes of vitamin B12, iodine and EPA + DHA). Our findings
do not indicate that vegetarian (without seafood) or vegan diets (without
seafood and dairy) cannot be nutritionally adequate. It means that solutions for
diets that are entirely or almost entirely plant-based should rely on additional
food products than those presently consumed by the general population, including
fortified foods (50–52). This warrants further studies about the potential of
new foods to extend the limit of the %PP range identified as adequate here.

Within the wide range of nutrient-adequate %PP values, we did not find a single
optimal diet, but a large range of diets with %PP from 25 to 70%. These diets
were all optimal when considering their health value, because their food
consumptions complied with minimum-risk exposure levels. These consisted of no
red meat and high levels of fruits and vegetables, whole grains, legumes, nuts
and milk, in line with dietary guidelines (53). Modeled healthy diets were
variations of this pattern, which explains why they were also similarly distant
from current diets. Within this healthy pattern spectrum, the increase in %PP
was predominantly related to the decrease in total and animal proteins. This
occurred mostly in poultry and eggs and, to a lesser extent, dairy. This finding
aligns well with the current spectrum of observed diets, with plant-based diets
being higher in plant protein but especially low in total and animal protein
(54, 55). This could simply be ascribed to the higher protein density in animal
protein sources compared to plant protein sources. Also, the nutrients
identified as limiting at the borders of the healthy %PP range appear to be
related to the nutrient density of animal vs. plant protein sources when
expressed relative to protein density. However, the dietary protein amount was
never limiting, even at the highest %PP levels. There is a growing consensus
that the protein package and not the protein per se are important to the
question of plant to animal protein ratio in the diet (6, 9). Likewise,
indispensable amino acid amounts were well above reference values based on
requirements. It is usually considered that dietary proteins, and in particular
plant proteins tend to complement each other, because dietary proteins are not
low in the same amino acids (56, 57). Lysine, which is the most critical amino
acid, and is specifically low in grains is not limiting in the diet if grains
are not the main source of protein in the diet (39). In real diets, composed of
a mix of different types of proteins that complement each other, sufficient
amounts of protein appear to guarantee sufficient amounts of amino acids (22,
55, 58).

Distance from the prevailing diets is often used in diet modeling to take into
account so-called cultural acceptability (59–61), also referred to as dietary
inertia (62). In this study, healthy diets in the 35–65% %PP range departed
rather similarly from the prevailing diets, which are still at ~35% %PP. This
confirms that the plant to animal protein ratio is, by itself, a poor descriptor
of diet characteristics, and so blanket statements about the right %PP are not
warranted. Given that modeled healthy diets ranging from 35% %PP (the level of
the current diets in Western countries) to 65% %PP were all very distant from
current diets, our study also shows that overcoming dietary inertia is required
for healthy diets, irrespective of the plant to animal protein target ratio
(63).

The GHGe and overall composite score for environmental pressures were lower for
healthy modeled diets than observed diets, and all the more as %PP increased. A
large body of literature has reported that diets which are more plant-based are
associated with lower environmental pressure, and vice versa, whether diets were
modeled (48, 61, 64, 65), observed (66–68) or composite (25). However, until our
study, this relationship had not yet been shown according to %PP in healthy
diets. In our setting, %PP was strongly associated with the environmental impact
of healthy diets. As compared to the prevailing diets, lower GHGe and composite
score are firstly explained by the removal of total red meat in all healthy
diets, red meat accounting for ~1/3 of the pressure in prevailing diets. This is
in line with the literature that points to red meat and associated
sustainability concerns (65, 69). Finally, we found that other environmental
pressures (land use and fossil resource use), except water use, had similar
patterns of change, in line with the literature (21, 48). The general
relationship between %PP and environmental pressure can mostly be ascribed to
the fact that animal sources are rich in protein, and that livestock breeding is
associated with higher resource use, higher land use, and higher GHGe (23,
70–72). Nevertheless, further investigation of the relationship between %PP and
environmental impacts would require prioritizing the minimization of
environmental impacts over that of diet departure. Therefore, we cannot rule out
the possibility that moderate %PP diets, if well-designed, may have as low
environmental impacts as high %PP diets, at the cost of a larger diet departure.

This study has some limitations. We modeled diets according to changes in
intakes of food groups, based on the present food repertoire and current intake
levels in the population. Food grouping is critical in diet modeling (33), and
food diversity and composition can change rapidly in Western countries, as seen
by recent changes (73). A similar limitation applies to the assessment of a
diet’s environmental impacts, for which also we did not consider variations
related to food production systems (74, 75). Nevertheless, we used a classical
food grouping, which helps represent dietary patterns at an appropriately high
level of detail. We also believe that using standard/traditional foods in
modeling provides a good starting point to evaluate the situation before
considering changes in the food offer or food composition. Our study uses
sources of information as background parameters, including references/targets
for nutrients and food categories. Clearly, there are many uncertainties in this
regard (33). Nonetheless, we believe that a strength of our study is our use of
a conceptual framework that aggregates most of the state of the art knowledge in
nutrition.

To conclude, we identified that the range of equally optimal %PP values for
nutrition and health is wide (25–70%), and that all of these healthy diets
deviate greatly from prevailing diets. From a public health perspective, there
is no unique, optimal %PP value when considering nutrition and health alone.
However, significant changes in current eating habits are nonetheless required
to achieve healthier diets. The focus should therefore shift from protein per se
to what is carried with protein (i.e., the nutrient package), the overall health
value of the food groups that convey protein, as well as the efforts needed to
move away from current Western dietary patterns (22). Moreover, in the higher
end of the adequate %PP range, modeled healthy diets have a lower environmental
impact and are thus more sustainable than other healthy diets. Thus, in current
and future dietary transitions, environmental pressures appear to be a more
direct determinant than health objectives to justify increasing %PP levels. At
%PP > ~80%, changes in food repertoire diversity, food composition, nutrient
enrichment or nutrient supplementation are required for fully nutrient-adequate
diets. Finally, the adequate %PP range may be narrower in some populations, such
as the elderly, who may have higher protein requirements than the general adult
population, and this would deserve further study.


PREPRINT

A manuscript was deposited as a preprint, to MedRxiv
(10.1101/2022.05.20.22275349). The copyright holder for this preprint is the
author, with all rights reserved and no reuse allowed without permission.


DATA AVAILABILITY STATEMENT

The raw data supporting the conclusions of this article will be made available
by the authors, without undue reservation.


AUTHOR CONTRIBUTIONS

HF and FM designed the research, wrote the first draft of the manuscript, and
had primary responsibility for the final content. HF conducted the research and
analyzed the data. AD, EP, FM, JW, J-FH, and EK-G provided methodological
support and help with interpretation of the results. All authors provided
critical comments on the manuscript, and read and approved the final manuscript.


FUNDING

This research did not receive any specific grant from funding agencies in the
public, commercial, or not-for-profit sectors.


ACKNOWLEDGMENTS

The authors thank Vincent Colomb and Mélissa Cornélius (Ademe) for their
important support in the use of the AGRIBALYSE database.


CONFLICT OF INTEREST

HF has received a research grant by INRAE from Roquette; FM has received
research grants as PhD fellowships under his direction by AgroParisTech and
INRAE from Terres Univia and Ecotone foundation, under the aegis of Fondation de
France.

The remaining authors declare that the research was conducted in the absence of
any commercial or financial relationships that could be construed as a potential
conflict of interest.


PUBLISHER’S NOTE

All claims expressed in this article are solely those of the authors and do not
necessarily represent those of their affiliated organizations, or those of the
publisher, the editors and the reviewers. Any product that may be evaluated in
this article, or claim that may be made by its manufacturer, is not guaranteed
or endorsed by the publisher.


SUPPLEMENTARY MATERIAL

The Supplementary material for this article can be found online at:
https://www.frontiersin.org/articles/10.3389/fnut.2023.1178121/full#supplementary-material


ABBREVIATIONS

ANSES, French Agency for Food, Environmental and Occupational Health and Safety;
CIQUAL, French Information Centre on Food Quality; DALYs, Disability-adjusted
life-years; DD, Diet departure criterion; GBD, Global Burden of Diseases; GHGe,
greenhouse gas emissions; HR, Health risk criterion; INCA3, Third Individual and
National Study on Food Consumption French Survey; %PP, Percentage of plant
protein in the diet; TMREL, Theoretical minimum risk exposure level.


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Keywords: healthy dietary patterns, nutrient adequacy, environmental footprints,
diet optimization, plant-based diets

Citation: Fouillet H, Dussiot A, Perraud E, Wang J, Huneau J-F, Kesse-Guyot E
and Mariotti F (2023) Plant to animal protein ratio in the diet: nutrient
adequacy, long-term health and environmental pressure. Front. Nutr. 10:1178121.
doi: 10.3389/fnut.2023.1178121

Received: 02 March 2023; Accepted: 18 May 2023;
Published: 15 June 2023.

Edited by:

Rui Poínhos, University of Porto, Portugal

Reviewed by:

Anne Pihlanto, Natural Resources Institute Finland (Luke), Finland
Amanda Gomes Almeida Sá, Federal University of Santa Catarina, Brazil

Copyright © 2023 Fouillet, Dussiot, Perraud, Wang, Huneau, Kesse-Guyot and
Mariotti. This is an open-access article distributed under the terms of the
Creative Commons Attribution License (CC BY). The use, distribution or
reproduction in other forums is permitted, provided the original author(s) and
the copyright owner(s) are credited and that the original publication in this
journal is cited, in accordance with accepted academic practice. No use,
distribution or reproduction is permitted which does not comply with these
terms.

*Correspondence: Hélène Fouillet, helene.fouillet@agroparistech.fr; François
Mariotti, francois.mariotti@agroparistech.fr



Disclaimer: All claims expressed in this article are solely those of the authors
and do not necessarily represent those of their affiliated organizations, or
those of the publisher, the editors and the reviewers. Any product that may be
evaluated in this article or claim that may be made by its manufacturer is not
guaranteed or endorsed by the publisher.



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