Received: 8 May 2020 | Revised: 7 July 2020 | Accepted: 14 July 2020

DOI: 10.1002/fsn3.1809

ORIGINAL RESEARCH

Comprehensive overview of the quality of plant- And animal-

sourced proteins based on the digestible indispensable amino
acid score

Laure Herreman | Paul Nommensen | Bart Pennings | Marc C. Laus

Avebe Innovation Center, Groningen,

The Netherlands Abstract
Indispensable amino acid (IAA) composition and standardized ileal digestibility (SID)
Correspondence
Laure Herreman and Marc C. Laus, of five animal- and 12 plant-based proteins were used to calculate their respective
Innovation Center, Groningen, 9747 AA, Digestible Indispensable Amino Score (DIAAS) according to the three age catego-
The Netherlands.
Emails: [email protected] (LH); ries defined by the Food and Agriculture Organization (FAO). Mean IAA content and
[email protected] (MC. L) mean SID obtained from each protein dataset were subsequently used to simulate
optimal nutritional quality of protein mixtures. Datasets revealed considerable vari-
ation in DIAAS within the same protein source and among different protein sources.
Among the selected protein sources, and based on the 0.5- to 3-year-old reference
pattern, pork meat, casein, egg, and potato proteins are classified as excellent qual-
ity proteins with an average DIAAS above 100. Whey and soy proteins are classified
as high-quality protein with an average DIAAS ≥75. Gelatin, rapeseed, lupin, canola,
corn, hemp, fava bean, oat, pea, and rice proteins are classified in the no quality claim
category (DIAAS <75). Potato, soy, and pea proteins can complement a broad range
of plant proteins, leading to higher DIAAS when supplied in the form of protein mix-
tures and at specific ratios. Such complementarity highlights the potential to achieve
an optimal nutritional efficiency with plant proteins alone.

KEYWORDS
DIAAS, digestibility, essential amino acids, sustainability, vegetable protein

1 | I NTRO D U C TI O N increasing in developing countries (Godfray et al., 2018). While

it has been recommended to shift global protein consumption to-
New protein sources have emerged in recent years to support the ward plant-based proteins (Boland et al., 2013; Pyett, Vet, Trindade,
transition toward more sustainable food production dedicated to Zanten, & Fresco, 2019), attention should be paid to the nutritional
human nutrition. Animal-sourced proteins, for example, from milk quality of new and alternative protein sources.
and meat, have shown to have a substantial impact on greenhouse Dietary protein quality is primarily characterized by their in-
gases and are known to contribute to depletion of natural sources dispensable amino acid (IAA) content. IAAs cannot be synthe-
(Aiking, 2014; Godfray et al., 2018). These proteins are included to tized by the human body and must be obtained from the diet. The
a large extent in Western diets, and their consumption is gradually current standard to evaluate the nutritional quality of proteins is

This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium,
provided the original work is properly cited.
© 2020 The Authors. Food Science & Nutrition published by Wiley Periodicals LLC.

Food Sci Nutr. 2020;8:5379–5391.  www.foodscience-nutrition.com | 5379

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5380 HERREMAN et al.

the Protein Digestibility Corrected Amino Acid Score (PDCAAS). 2 | M ATE R I A L S A N D M E TH O DS

Due to several drawbacks of this method (Sarwar, 1997), the Food
and Agriculture Organization (FAO) recommends another proce- 2.1 | Data collection from the literature
dure called Digestible Indispensable Amino Acid Score (DIAAS)
(FAO, 2013). DIAAS addresses the limitations of the PDCAAS Five animal (whey, casein, egg, gelatin, and pork meat) and 12
method by considering the ileal digestibility of individual amino plant protein sources (soy, pea, lupin, fava bean, rapeseed, canola,
acids (AAs), with the growing pig as preferred model over the rat, hemp, wheat, potato, oat, rice, and corn) were selected, based
and by avoiding truncation of the score obtained. Furthermore, on their occurrence in the Western diet or by the growing inter-
reactive digestible lysine rather than total digestible lysine should est in the vegetarian, vegan, or flexitarian markets. Growing pig
be considered to determine the DIAAS of processed and cooked intervention studies providing complete IAA composition, crude
foods. The FAO DIAAS report also recommends classification of protein content (CP), and IAA standardized ileal digestibility (SID)
proteins using quality categories based on the DIAAS value: <75 were selected.
(no quality claim); 75–99 (high-quality protein); and ≥100 (excellent
quality protein). The FAO has updated the age-related AA refer-
ence scoring patterns and recommends that the general population 2.2 | DIAAS of a single protein source
be categorized according to three distinct age-related reference
patterns: 0–6 months (infant), 0.5–3 years (children), and > 3 years The most limiting digestible indispensable amino acid content (DIAA)
(rest of the population). defines the DIAAS value of a protein. DIAA ratios were determined
Recent studies compared various protein sources based on their according to the three reference pattern scores defined by FAO:
AA composition (Gorissen et al., 2018; Sá, Moreno, & Carciofi, 2020; infant (0–6 months), children (0.5–3 years), and children older than
van Vliet, Burd, & van Loon, 2015). However, these data do not in- 3 years, adolescents, and adults (FAO, 2013).
form to which extent a specific protein can be digested to meet the For a given IAA “y,” DIAA ratio is calculated as follows:
human body requirements. The most extensive studies to date pro-
vide DIAAS values of eight protein sources (Cervantes-Pahm, Liu, & IAAy × SIDy
DIAAy ratio = (1)
Stein, 2014; Mathai, Liu, & Stein, 2017). To broaden the comparison Reference pattern score IAAy
of DIAAS to more protein sources, IAA profiles and IAA standard-
ized ileal digestibility (SID) data were used to calculate the DIAAS where IAA y is expressed as mg/g CP.
values of 17 protein sources according to the three reference scoring The lowest DIAA ratio leads to the DIAAS value of a protein:
patterns.
Standardized ileal digestibility is preferred over apparent ileal DIAAS = 100 × lowest DIAA ratio among IAAs (2)
digestibility (AID) since the latter does not correct for the AA en-
dogenous loss inherent to the body function (Stein, Sève, Fuller, Mean DIAAS values were obtained from the lowest mean DIAA for
Moughan, & de Lange, 2007). Endogenous AAs are secreted into the each protein source. Graphs were generated with Microsoft Excel
small intestine, and an estimated 20%–35% is not reabsorbed by the Office 365 and Minitab software version 18.1.
body before reaching the distal ileum (de Lange, Sauer, Mosenthin,
& Souffrant, 1989; Souffrant et al., 1993). Applying AID as digest-
ibility coefficient therefore leads to underestimation of the actual 2.3 | DIAAS of protein mixtures
AA digested. We also combine protein sources to optimize their
nutrition profile, for which protein digestibility coefficients must be Digestible indispensable amino acid content of protein mixtures
additive. SID therefore provides a more accurate and appropriate were calculated as detailed by FAO and according to the reference
measurement of the AA ileal digestibility of single protein sources or pattern score of 0.5- to 3-year-old population group (FAO, 2013).
protein mixtures (Stein, Pedersen, Wirt, & Bohlke, 2005). To improve Average values of single proteins for IAAy and SIDy were used
comparison between results, studies involving rodents, gilts, sows, to estimate the DIAAys of protein mixtures. The latter is written
piglets, weanling pigs, and finishing pigs were excluded and instead as a linear combination with respect to the mixing ratios Ri. For
only data obtained with growing pigs were used. In addition, only a mixture of protein 1 (P1), protein 2 (P2) up to protein n (Pn), this
protein material containing at least 10% crude protein, and falling in results in:
categories such as seeds, meals, flours, concentrates, and isolates,
DIAAy = cy,1 × R1 + cy,2 × R2 + ⋯ + cy,n × Rn (3)
was included in the investigation. Material in the forms of hulls,
brans, or peels was excluded, being less suitable sources of protein
for human consumption. The obtained datasets were subsequently where:
used to simulate protein mixtures and highlight the complementarity
of proteins at specific ratios to obtain higher values than that of the IAAyi × SIDyi
cy,i = (4)
individual proteins. Reference pattern score IAAy
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HERREMAN et al. 5381

TA B L E 1 Datasets collected to
Number of
calculate DIAAS of protein sources
Protein source datasetsa References

Wheat 37 Cervantes-Pahm et al., (2014); CVB, (2016); Lee, Ahn,

Son, & Kim, (2019); Mathai et al., (2017); McGhee &
Stein, (2018); NRC, (2012); Pedersen et al., (2007);
Sauvant et al., (2004); Wang, Osho, & Adeola, (2018);
Woyengo et al., (2014); Zhao et al., (2019)
Rice 3 CVB, (2016); Gottlob et al., (2006)
Oats 8 Abelilla, Liu, & Stein, (2017); Cervantes-Pahm
et al., (2014); CVB, (2016); NRC, (2012); Sauvant
et al., (2004)
Rapeseed 31 CVB, (2016); Huang et al., (2018); Hulshof et al., (2016);
Li et al., (2015); Maison & Stein, (2014); Sauvant
et al., (2004)
Pea 22 CVB, (2016); Grosjean et al., (2000); Mathai
et al., (2017); NRC, (2012); Sauvant et al., (2004); Stein
& Bohlke, (2007)
Soy 43 Baker & Stein, (2009); Berrocoso et al., (2015);
Cervantes-Pahm & Stein, (2008); CVB, (2016); Hulshof
et al., (2016); Kong, Kang, Kim, & Kim, (2014); Lee
et al., (2019); Mathai et al., (2017); NRC, (2012);
Sauvant et al., (2004); Son, Park, Park, & Kim, (2019)
Whey 12 CVB, (2016); Gottlob et al., (2006); Mathai et al., (2017);
NRC, (2012); Sauvant et al., (2004)
Casein 2 CVB, (2016); NRC, (2012)
Egg 3 Woyengo et al., (2015); Zhang et al., (2015)
Canola 26 Berrocoso et al., (2015); Liu et al., (2016); Liu, Song,
Maison, & Stein, (2014); Maison & Stein, (2014);
NRC, (2012); Park, Ragland, Helmbrecht, Htoo,
& Adeola, (2019); Seneviratne et al., (2010); Son
et al., (2019); Wang et al., (2018); Xue, Ragland, &
Adeola, (2014)
Corn 44 Almeida, Petersen, & Stein, (2011); CVB, (2016); Ji, Zuo,
Wang, Li, & Lai, (2012); Lee et al., (2019); NRC, (2012);
Sauvant et al., (2004); Son et al., (2019); Xue
et al., (2014); Zhang et al., (2019)
Potato 5 Beelen G.M., (1999); CVB, (2016); NRC, (2012); Sauvant
et al., (2004)
Hemp 1 Presto, Lyberg, & Lindberg, (2011)
Gelatin 3 NRC, (2012); Petersen, Smiricky-Tjardes, & Stein, (2005)
Lupin 4 CVB, (2016); Lee et al., (2019); NRC, (2012)
Fava bean 3 NRC, (2012); Sauvant et al., (2004)
Pork 9 Bailey & Stein, (2019)
a
Each dataset combines complete amino acid composition of the protein (% CP) and standardized
ileal digestibility of the nine indispensable amino acids (including cysteine and tyrosine).

and For a mixture of two protein sources, Equation (3) can be rewrit-
ten by applying R 2 = 1 - R1:
Mi
Ri = ∑ (5)
Mi (6)
( )
DIAAy = cy,1 − cy,2 × R1 + cy,2

Note that Equation (4) is independent of material crude protein The optimal mixture provides the maximum DIAAS among all
content. Mi is the amount of pure protein from protein source i. By possible ratios. The corresponding R1 value was determined with
using pure protein, DIAAy remains independent of the protein con- the Solver tool available in Microsoft Excel, using the constraint
tent of individual material used in the mixture. 0 ≤ R1 ≤ 1. The objective was set to find the highest DIAAS ≤ 100.
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5382 HERREMAN et al.

For a mixture of three protein sources, a similar scheme was quality categories (<75, no quality protein claim; 75–99, high-quality
used: protein claim; and ≥100, excellent quality protein claim), while scores
of wheat, rapeseed, lupin, pea, potato egg, and canola proteins fall
DIAAy = cy,1 × R1 + cy,2 × R2 + cy,3 × R3 (7) in two of the quality categories. This is further highlighted with the
broad absolute DIAAS variations observed within most protein data-
And using R3 = 1 - R1 - R 2, this results in: sets. Based on the 0.5- to 3-year-old scoring pattern, DIAAS values
of wheat, rapeseed, and corn proteins display the greatest disparity
(8) with respective DIAAS ranges of 53, 43, and 44. DIAAS variation
( ) ( )
DIAAy = cy,1 − cy,3 × R1 + cy,2 − cy,3 × R2 + cy,3
tends to decrease for the infant group (0–0.5 years old), with range
The values of R1, R 2, and R3 for the optimal mixture were also cal- values of 32, 20, and 34 for wheat, rapeseed, and corn proteins, re-
culated with the Solver tool available in Microsoft Excel. Equation (8) spectively. Such decreases in variation can be explained by higher
was optimized by modifying both R1 and R 2. Values of R1 and R 2 IAA requirement expressed in the scoring pattern and the shift in
were constrained to 0 ≤ R1 ≤ 1 and 0 ≤ R 2 ≤ 1 with the objective to limiting amino acid as detailed in Table S2.
find the highest DIAAS ≤ 100. Given the varying protein content among protein sources, the
Similar to Equation (2), the DIAAS score is obtained from the absence of measurements of antinutritional factors (ANFs), and the
lowest DIAA value of the protein mixture: limited description of the process used to obtain the various protein
sources, a selection cannot be based on a specific determinant. For
DIAAS (P1 + P2 + … + Pn ) = 100 × lowest DIAA (P1 + P2 + … + Pn ) (9) this reason, the average DIAAS value obtained from each protein
dataset was selected.
3 | R E S U LT S

3.1 | DIAAS variation within protein datasets 3.2 | DIAAS per protein source

Studies providing complete IAA composition, CP content, and IAA Mean DIAAS values obtained from the lowest average DIAA re-
SID were selected (Table 1). The amount of data available from the veal large differences among plant-derived proteins, varying from
literature varies according to the protein source. Digestibility of 36 ± 14.9 (corn) to 100 ± 7.3 (potato), and among animal-derived
corn, soy, canola, and wheat proteins has been extensively studied proteins, varying from 2 ± 3.0 (gelatin) to 117 ± 11.7 (casein), con-
in growing pigs, evidenced by the relatively large number of data- sidering the scores obtained for 0.5- to 3-year-old group (Table 2).
sets obtained through numerous references (Table 1 and Table S1). For this age group, the limiting amino acid of protein obtained from
Contrarily, complete data on ileal digestibility of amino acids from cereal grains—such as corn, wheat, hemp, rice, canola, oat, rape-
hemp and casein are limited to 1 and 2 datasets, respectively. seed—is lysine (Lys), while the leguminous sources of protein (fava
Each retrieved dataset was used to obtain the DIAAS value ac- bean, pea, lupin, soy) are limited by the sulfur-containing amino
cording to the three scoring patterns. As displayed in Figure 1, DIAAS acids methionine and cysteine (Met + Cys). Potato protein, which
values are scattered across the different protein quality categories interestingly shows a high DIAAS value, is derived from a tuber-
for many protein sources. Based on the 0.5- to 3-year-old scoring ous plant and therefore does not belong to any of these categories
pattern, soy and wheat proteins possess DIAAS values in all three (Table 2).

F I G U R E 1 Variation in DIAAS
obtained from SID and IAA data available
from pig intervention studies. DIAAS
calculated for each scoring pattern
as defined by FAO (2013): infant
(0–0.5 years), children (0.5–3 years), and
children older than 3 years, adolescents,
and adults
 HERREMAN et al.

TA B L E 2 Digestible indispensable amino acid scores of various protein sources according to the 0.5-to 3-year-old reference pattern score

Limiting
Protein source Histidine Isoleucine Leucine Lysine Met + Cys Phe + Tyr Threonine Tryptophan Valine DIAAS AAa

Corn 110 ± 29.7 90 ± 14.6 162 ± 58.2 36 ± 14.9 126 ± 22.2 140 ± 42.8 86 ± 10.2 52 ± 35.4 90 ± 14.4 36 Lys
Rice 93 ± 7.0 89 ± 17.4 80 ± 12.4 47 ± 2.3 104 ± 11.0 119 ± 29.6 75 ± 4.1 114 ± 28.6 95 ± 18.0 47 Lys
Wheat 118 ± 21.7 91 ± 10.5 87 ± 11.1 48 ± 10.6 127 ± 19.4 109 ± 16.9 78 ± 7.1 127 ± 17.8 92 ± 9.8 48 Lys
Hempb 124 ± NA 106 ± NA 85 ± NA 54 ± NA 121 ± NA 131 ± NA 87 ± NA - 99 ± NA 54 Lys
Fava bean 108 ± 4.1 106 ± 2.2 95 ± 5.4 95 ± 4.3 55 ± 5.1 119 ± 3.4 91 ± 6.2 68 ± 7.8 83 ± 2.2 55 Met + Cys
Oat 91 ± 11.4 100 ± 4.2 94 ± 4.9 57 ± 5.8 151 ± 52.9 135 ± 9.2 85 ± 5.9 110 ± 17.2 102 ± 3.4 57 Lys
Rapeseed 107 ± 8.0 90 ± 4.9 78 ± 5.0 67 ± 10.3 125 ± 14.3 92 ± 12.3 97 ± 6.5 106 ± 9.4 92 ± 4.6 67 Lys
Lupin 121 ± 16.1 104 ± 27.2 89 ± 19.3 75 ± 12.3 68 ± 12.7 121 ± 35.6 97 ± 22.7 72 ± 22.5 78 ± 14.6 68 Met + Cys
Pea 99 ± 9.7 101 ± 13.1 87 ± 11.5 110 ± 10.8 70 ± 12.3 116 ± 16.3 94 ± 7.9 77 ± 7.1 83 ± 9.8 70 Met + Cys
Canola 105 ± 6.9 93 ± 9.9 79 ± 7.8 72 ± 9.2 121 ± 10.4 97 ± 6.1 97 ± 12.2 112 ± 19.5 87 ± 9.1 72 Lys
Soy 119 ± 9.4 124 ± 8.3 102 ± 6.1 96 ± 9.0 91 ± 11.5 147 ± 8.3 105 ± 6.0 132 ± 21.1 95 ± 7.3 91 Met + Cys
Potato 100 ± 7.3 156 ± 9.2 143 ± 11.2 122 ± 4.6 115 ± 6.0 210 ± 18.2 165 ± 12.0 128 ± 13.7 138 ± 5.1 100 NA
Gelatin 34 ± 9.5 34 ± 10.6 35 ± 8.7 60 ± 11.5 27 ± 10.3 36 ± 13.0 46 ± 4.9 2 ± 3.0 46 ± 8.6 2 Trp
Whey 85 ± 10.8 166 ± 23.2 138 ± 22.9 131 ± 25.2 132 ± 21.6 101 ± 14.0 174 ± 22.8 180 ± 47.0 116 ± 14.3 85 His
Egg 101 ± 11.7 129 ± 25.5 103 ± 16.2 133 ± 58.4 123 ± 53.2 144 ± 18.9 106 ± 14.1 129 ± 49.7 105 ± 32.3 101 NA
Casein 147 ± 9.4 153 ± 4.3 141 ± 6.6 134 ± 4.3 117 ± 5.0 201 ± 8.0 130 ± 4.3 159 ± 13.4 148 ± 2.7 117 NA
Pork 197 ± 13.6 153 ± 11.1 122 ± 9.2 157 ± 10.7 128 ± 10.7 148 ± 10.4 145 ± 10.1 144 ± 17.1 117 ± 9.0 117 NA

Note: Data expressed as mean of individual DIAA values ± standard deviation.

a
Limiting AA when DIAAS <100, NA not applicable when DIAAS ≥100.
b
Dataset does not include tryptophan measurements. This is however the only publication reporting the ileal digestibility of hemp in pig studies. These data were therefore included for comparison.
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5384 HERREMAN et al.

Due to different protein requirements between age groups, proteins. The degree of complementarity depends on the ratio of the
the limiting amino acid of the protein sources varies per age group. combined protein sources, as illustrated in Figure 3.
Tryptophan (Trp), lysine (Lys), and phenylalanine and tyrosine Multiple simulations were used to calculate the maximum DIAAS
(Phe + Tyr) are the most common limiting IAAs for infants (Table of mixtures according to Equations (6), (8), and (9), enabling mix-
S2). In this population group, maximum scores are obtained for tures such as oat/lupin, fava bean/corn, and pea/wheat to reach the
casein (86 ± 17.5), followed by pork meat (72 ± 8.6) and potato high-quality protein range (Table 3). Not all leguminous/cereal pro-
protein (67 ± 3.3) (Figure 2). The most limiting IAAs for children, tein combinations will lead to higher scores: If Lys is the second or
adolescents, and adults (>3 years old) are Lys, Met + Cys, and histi- third limiting IAA in leguminous protein, the DIAAS increase will be
dine (His) for cereal, leguminous, and potato proteins, respectively minimal. This is the case of lupin protein scoring 75 for Lys (Table 2).
(Table S3). Among these mixtures, potato protein shows the ability to increase
A protein source reaching a DIAAS of 100 or above indicates the DIAAS of most plant protein sources to 100. In combination with
that none of its amino acids is limiting and this sole protein source casein, egg protein, or pork meat, most plant proteins can reach a
should be able to meet physiological requirements. Among the DIAAS of 100 until a certain ratio is reached (Table S4).
proteins selected in this study, potato protein, egg protein, casein,
and pork meat reach this level based on the 0.5- to 3-year-old ref-
erence pattern. For a protein source with a DIAAS lower than 100, 4 | D I S CU S S I O N
different strategies are possible to ensure an adequate protein in-
take based on such protein. A first option is to increase the protein 4.1 | Factors influencing DIAAS variability
intake of the limiting protein until the physiological requirement is
reached. Higher protein intake has indeed shown to increase amino Protein IAA content and SID coefficients were used to determine
acid uptake in plasma (Gorissen et al., 2016). For example, based DIAAS values for 17 protein sources. Broad absolute DIAAS vari-
on the selected datasets, less than three portions of corn protein ations can be observed within most protein datasets. This can be
(2.8*36 = 101) would theoretically be needed to meet these require- attributed to the type of material fed to the growing pigs.
ments while 1.45 portions of pea protein (1.45*70 = 101) would be Genotype or cultivar considerably influences AA content,
required. A second option is to combine protein sources and ensure AA composition, and SID (Spindler et al., 2016; Strang, Eklund,
complementarity of their amino acids to reach a higher DIAAS. Rosenfelder-Kuon, Htoo, & Mosenthin, 2017; Zhao et al., 2019).
Similarly, the content of antinutritional factors (ANFs), for exam-
ple, glycoalkaloid, glucosinolates, protease inhibitors, phytate, and
3.3 | Toward a higher DIAAS with protein saponins, differs among genotypes (Oomah et al., 2011; Sharma,
combinations Kaur, Goyal, & Gill, 2014). Along with processing conditions, ANFs
are well-known to influence plant protein digestibility (Sá, Moreno,
The digestibility score of each indispensable amino acid highlights & Carciofi, 2019; Sarwar Gilani, Wu Xiao, & Cockell, 2012). For in-
the potential of complementarity between protein sources (Table 2). stance, Luo et al. (Luo & Xie, 2013) reported that phytate and tryp-
Cereal-based proteins, scoring low in Lys but high in Met + Cys, can sin inhibitor contents increase with dehulling of fava beans, but was
to some extent complement leguminous proteins, scoring high in most effectively reduced by first soaking the beans before dehulling
Lys but low in Met + Cys. Potato protein, which scores higher than followed by an autoclaving step. Pastuszewska et al. (Pastuszewska,
100 for each DIAA value, can also serve to increase DIAAS of many Tuśnio, Taciak, & Mazurczyk, 2009) also highlighted the variations

F I G U R E 2 Average DIAAS of
various protein sources according to the
three reference pattern scores: infant
(0–0.5 years), children (0.5–3 years), and
children older than 3 years, adolescents,
and adults. Error bars represent standard
deviation
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HERREMAN et al. 5385

F I G U R E 3 Variation in digestible
indispensable amino acid values and
resulting DIAAS in pea/rice protein
mixture. Illustration based on the average
SID and average IAA composition
obtained from pea protein and rice protein
datasets. A maximum DIAAS of 84 can
be obtained when 41% rice protein is
composing the pea/rice protein mixture as
indicated by the blue arrow

TA B L E 3 Improved DIAAS as a result of optimal plant protein reduce the content of ANFs leading to an increased AA digestibility
combination in young pigs (Zhang et al., 2013). In the studies selected for this

Plant protein Max. DIAASa analysis, the diverse processes used to obtain the protein materi-
mixture (≤100) Ratio als—such as specific heat treatment, solvent extraction conditions,
or enzymatic reaction—are not consistently described; the resulting
Oat/lupin 76 7/93
activity of ANFs is rarely investigated. Moreover, many of the data-
Oat/lupin/soy 91 10/10/80
sets used in the current study are based on raw feed ingredients.
Oat/lupin/potato 100 10/20/60
Such material often displays a higher ANF content and ANF activity
Fava bean/corn 64 75/25
than dietary protein used in food products. Feedstuffs in their raw
Fava bean/corn/soy 85 10/20/70
state do not reflect the processed and cooked forms of food used
Fava bean/corn/potato 100 15/20/65 for human consumption. Processing and especially cooking can con-
Fava bean/rapeseed 82 55/45 siderably affect amino acid composition and digestibility of proteins,
Pea/wheat 85 60/40 resulting in a different DIAAS (Bailey, Mathai, Berg, & Stein, 2019;
Pea/wheat/soy 90 25/20/55 Friedman, Gumbmann, & Masters, 1984). While heat treatment can
Pea/wheat/potato 100 25/25/50 inactivate some of the ANFs, it can also induce molecular alterations
Canola/pea 84 35/65 making the protein more resistant to the action of digestive pro-
Canola/pea/soy 92 25/15/60 teases or on the contrary more accessible (Carbonaro, Cappelloni,

Canola/pea/potato 100 35/35/30 Nicoli, Lucarini, & Carnovale, 1997; Duodu, Taylor, Belton, &
Hamaker, 2003; Liu, Zheng, & Chen, 2019). This is also illustrated in
Soy/canola 92 85/15
the present study in which pea protein obtains an average DIAAS of
Soy/wheat 90 90/10
70 while after extrusion its DIAAS can increase to 82 or 86 depend-
Soy/wheat/potato 100 25/20/55
ing upon the extrusion temperature (Table S2).
Soy/oat 92 90/10
Besides digestibility, amino acid composition of cooked protein
Corn/potato 100 25/75
food can differ greatly from that of its raw state due to leaching of
Corn/soy 88 15/85 soluble protein fractions into the boiling liquid and through the for-
Wheat/potato 100 30/70 mation of amino acid derivatives (Carbonaro et al., 1997; Friedman
Lupin/potato 100 30/70 et al., 1984; Nierle, 1985; Struthers, 1981). With an altered amino
a
DIAAS value derived from average IAA content and average SID per acid composition, the DIAAS value of the cooked protein, and possi-
protein sources and calculated according to Equations (6), (8), and (9). bly its limiting amino acid, may differ strongly. Animal-based proteins
Based on 0.5- to 3-year-old reference pattern score. are also subjected to protein quality variation as a result of process-
ing. Whey protein is generally considered an excellent protein with
in the activity of solanidine glycoalkaloids and trypsin inhibitors in a DIAAS superior to 100, but surprisingly, multiple references led
potato protein concentrate among process conditions from various to DIAAS values ranging from 78 to 88 for whey-based products,
potato starch production sites. Furthermore, fermentation or en- implying that purity and the recovery process can be significant.
zymatic treatments of soybean have also shown their potential to This further illustrates the importance of considering processing
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5386 HERREMAN et al.

and cooking conditions when determining DIAAS. The present and Stein (Rayadurg & Stein, 2003) reported a linear decrease in ileal
study gathers a large DIAAS dataset of which only a few DIAAS endogenous losses of CP and most AAs as the diet increased from 1
are obtained from cooked products. In order to build a coherent to 3 times the maintenance requirement of growing barrows. Such
DIAAS value database, the protein intervention material, preferably reduced endogenous ileal AA losses will lead to a greater SID of AAs
cooked, and its processing conditions should be well characterized (Moter & Stein, 2004), eventually impacting the DIAAS value. This
to ensure transparency on the nutritional quality provided to human further highlights the importance of providing similar animal man-
consumption. agement conditions to obtain objective DIAAS values. Moreover,
Although findings based on hulls, brans, and peels were ex- three major animal feed databases (CVB, 2016; NRC, 2012; Sauvant,
cluded, remarkable difference can be observed in the purity of the Perez, & Tran, 2004) were included in our datasets, but distinctions
protein materials studied. Flours contain more fibers than protein between growing pigs, sows, finishing pigs, or piglets are not always
isolates or concentrates, thereby also influencing the protein digest- detailed, and this also likely contributes to the variation observed in
ibility (Mosenthin, Sauer, & Ahrens, 1994; Myrie, Bertolo, Sauer, & the collected data.
Ball, 2008). It is suggested that protein and nonstarch polysaccha- Overall, the differences in the setup of intervention studies high-
rides increase production of pancreatic juices and bile, and stimulate light the need for harmonized methods when determining growing
secretion of gut mucin protein composing the mucosal layer, thus pig SID. Harmonization might reduce the variation observed in the
contributing to higher ileal AA endogenous losses (Low, 1989; Morel, current investigation and would generate more reliable data for
Melai, Eady, & Coles, 2005). This indicates that applying endogenous plant proteins. These adjustments should be accompanied by a more
loss obtained from a N-free diet control group to the intervention detailed characterization of intervention material to ensure reliable
group could cause an underestimation of the amino acid SID of the DIAAS comparison between protein sources intended to human
studied protein material. True ileal digestibility (TID), also referred to consumption. Ideally, each food protein source should be classified
as real ileal digestibility, accounts for diet-specific endogenous AA into subcategories detailing their content in fibers, content of ANFs,
loss and is therefore more accurate. However, data based on TID and specific processing conditions.
remain scarce due to methodological complications involving such
measurement.
Variations observed within each DIAAS dataset can also orig- 4.2 | Distinctive DIAAS between protein sources
inate from the conditions in which the intervention diets were
provided. Firstly, clear dissimilarities can be noted in starting age/ Independent of the absolute variation in DIAAS observed for each
body weight of the growing pigs, varying from 17.8 ± 1.7 kg (Zhang protein source, the overall dataset reveals clear disparities in DIAAS
et al., 2015) to 76.2 ± 5.6 kg (Pedersen, Boersma, & Stein, 2007). between plant proteins. DIAAS of potato protein reaches the excel-
Several publications (Cunningham, Friend, & Nicholson, 1962; lent protein quality range (DIAAS ≥100) as defined by FAO, similar
Susenbeth, Dickel, Diekenhorst, & Höhler, 1999) reported a lower to most animal-derived proteins. Soy and whey proteins obtain a
CP digestibility in early growing pigs compared with both grow- DIAAS score above 75, defining them as high-quality protein. Corn,
ing and finishing-growing pigs. Likewise, younger gestating sows wheat, rice, fava bean, oat, and hemp proteins obtain average scores
showed a lower apparent crude protein digestibility than older ges- below 60. Plant proteins therefore clearly differ in terms of nutri-
tating sows (Jacyno et al., 2016). Based on similar results, Hennig tional profile, and nuances should accordingly be applied when com-
and colleagues (Hennig, Bock, Wünsche, & Kreienbring, 1979) sug- paring plant proteins to animal-derived proteins.
gested that endogenous loss could be of influence. This hypothesis Digestible Indispensable Amino Score value is determined by the
was confirmed by Nitrayova et al. (Nitrayová, Brestenský, Patráš, & most limiting digested IAA of the protein. IAA composition of a pro-
Heger, 2013), who reported an increased AA TID concomitantly with tein source thus has the majority influence on its DIAAS value. The
a lower AID in pigs of 20.6 kg compared to pigs with average weight discrepancies displayed in Figure 2 are for the most part inherent
of 64.7 kg. Young animals thus tend to produce higher endogenous to the IAA content of the protein and are clearly illustrated by gel-
AA loss than older pigs. Since SID is obtained by correcting AID with atin's score. High IAA content combined with low ileal digestibility
endogenous AA losses, SID coefficients will consequently increase can considerably impact DIAAS values, particularly if this involves
in younger animals. This suggests that neonatal pig and piglets could the most commonly limiting IAAs, Lys, or Met + Cys. Ileal digestibil-
be more suitable models to calculate the DIAAS values of the in- ity is influenced by several features of the protein. The amino acid
fant group than growing pigs (Buddington, Ja, Puchal-Gardiner, & sequence may influence the rate of hydrolysis by digestive prote-
Sangild, 2001; Moughan, Birtles, Cranwell, Smith, & Pedraza, 1992). ases. Gastric pepsin is known for its affinity with hydrophobic sites
Secondly, the daily amount of protein feed provided to the (Fruton, 1970) and its propensity to cleave after phenylalanine and
animals varies among studies. For instance, Cervantes-Pahm leucine residues (Powers, Harley, & Myers, 1977), while pancreatic
(Cervantes-Pahm et al., 2014) provided two times the maintenance trypsin favors basic amino acids (arginine and lysine) (Evnin, Vásquez,
energy requirement during intervention, while the diets in Liu et al. & Craik, 1990). Moreover, the protein secondary conformations
(Liu, Jaworski, Rojas, & Stein, 2016) and Berrocoso et al. (Berrocoso seem to hinder the accessibility of digestive proteases to cleaving
et al., 2015) included 3.4 times the estimated requirement. Rayadurg sites. High content of beta-sheet has been reported in soy protein
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HERREMAN et al. 5387

(>40%) (Herrero, Jiménez-Colmenero, & Carmona, 2009), peas protein content between protein sources to ensure the ratio would
(>40%) (Beck, Knoerzer, & Arcot, 2017), rice (44,9%) (Wang, Wang, solely be influenced by IAA content and SID of respective proteins. It
Wang, & Chen, 2016), wheat gluten (50%) (Tang et al., 2019), and oat is, however, advised to apply the specific CP of proteins in a case-by-
(36,8%–74%) (Liu et al., 2009; Zhao et al., 2017), while such structural case manner for the determination of DIAAS of a diet or developing
arrangement tend to account for less than 30% in milk-based protein food products. Many of the studies selected for these calculations
(Carbonaro, Maselli, & Nucara, 2012; Curley, Kumosinski, Unruh, & include protein sources with low average CP content such as oats
Farrell, 1998) and meat proteins (Herrero, Carmona, Lopez-Lopez, (18.3%), peas (26%), or fava beans (26.5%), contrary to potato pro-
& Jimenez-Colmenero, 2008). This relatively high proportion of be- tein (78.9%) and soy protein (49.5%). Mixtures based on potato pro-
ta-sheet conformations in leguminous and cereal-based proteins re- tein and soy protein therefore tend to generate mixtures richer in
sults in reduced protein in vitro digestibility (Carbonaro et al., 2012; protein, contributing to better nutritional efficiency.
Yang et al., 2016). Furthermore, multiple compounds present in plant The DIAAS method delivers a score characterizing the quality
proteins can interact with digestive enzyme by forming stable com- of protein sources. To date, most scores are obtained from single
plexes and impairing the enzymatic functionality, thereby inhibiting protein materials, while the protein digestibility is known to be influ-
protein digestion (Sarwar Gilani et al., 2012). As detailed earlier, it enced by food matrices and food preparation (Dupont, Le Feunteun,
can be prevented or reduced by suitable processing in the form of Marze, & Souchon, 2018). Lysine, one of the most commonly limit-
heat-induced denaturation, enzymatic reaction, or fermentation (Sá ing IAAs, is also one of the most reactive AAs (Hurrell, Carpenter,
et al., 2019; Sarwar Gilani et al., 2012). Sinclair, Otterburn, & Asquith, 1976). During thermal processing,
The vast majority of data used in this investigation are from chemical reactions between reducing sugars and lysine lead to for-
animal nutrition studies, that is, protein preparations intended for mation of Maillard reaction products. Such reactivity reduces the
animal feed. Protein products intended for human nutrition may dif- availability of lysine (Nyakayiru et al., 2020), hence the FAO recom-
fer in their processing and overall composition. New data on pro- mendation for the use of digestible reactive lysine instead of total
tein material that is specifically intended for food consumption are digestible lysine to determine the DIAAS. Such considerations will
therefore needed to confidently apply their DIAAS value to human greatly affect the DIAAS value of protein, and possibly its limiting
consumption. AA. For example, Hulshof et al. (Hulshof, Bikker, van der Poel, &
Hendriks, 2016) observed a 30%–40% decrease in reactive lysine
in soybean meal and rapeseed meal after a toasting step in the pres-
4.3 | Seeking nutritional efficiency ence of monosaccharides. A limitation of our study is the reliance
on total digestible lysine, as this is most commonly reported in the
The cause of disparities in DIAAS values appears multifactorial. literature. It is therefore also advised to investigate DIAAS values
Depending on the processing conditions, purity of the material, or of processed and/or cooked foods and consider their respective
feeding conditions, a protein DIAAS will vary, making the choice of digested reactive lysine to obtain a complete and reliable DIAAS
a representative product per protein source challenging. To further database. Furthermore, in recent years attention has increasingly
compare the DIAAS of protein sources, we therefore took an objec- focused on digestion kinetics and muscle anabolic properties of pro-
tive approach by considering the mean DIAAS values for the 0.5- to teins, triggered by bioavailable leucine (Casperson, Sheffield-Moore,
3-year-old population group. Although DIAAS expresses the quality Hewlings, & Paddon-Jones, 2012), but DIAAS values do not pro-
of protein based on its most limiting IAA score, it also highlights the vide information on these features. However, a higher DIAAS score
opportunity to combine the strength of different protein sources. does suggest good potential for increased net body protein utiliza-
The increased DIAAS values obtained from mixtures show the po- tion, although the latter must be confirmed by intervention studies
tential to achieve a protein nutritional efficiency with sustainable tracking net postprandial utilization of prepared foods combining
protein sources. Nutritional efficiency lies in meeting physiological various protein sources. Lastly, dietary protein quality should be
requirements with minimal intake of high-quality protein, as op- further evaluated along with their sustainability impact. The relative
posed to higher protein intake of low-quality protein. This last sce- contribution of dietary protein in meeting physiological amino acid
nario is not necessarily favorable due to a potentially high satiety requirement should perhaps be expressed according to their envi-
effect resulting in inadequate protein intake and suboptimal sustain- ronmental footprint, as recently highlighted by Tessari et al. (Tessari,
ability impact of such a diet. Potato protein has shown to be the most Lante, & Mosca, 2016).
promising source of plant protein to achieve nutritional efficiency:
With high scores obtained for every IAA, it can boost most mixtures
to the excellent protein quality category (DIAAS ≥100). Similarly, soy 5 | CO N C LU S I O N S
protein and pea proteins provide good potential to boost many cereal
proteins toward the high-quality protein category (DIAAS = 75–99). In conclusion, this investigation shows that protein quality based on
While simulating protein mixtures, crude protein content was not DIAAS differs not only between animal and plant proteins but also
taken into consideration due to the considerable variation among between plant protein sources. Based on the 0.5- to 3-year-old scor-
and between proteins. Equations (6) and (8) thus assume an identical ing pattern, potato and most animal-derived proteins tend to reach
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5388 HERREMAN et al.

the excellent protein quality category (DIAAS ≥100). Soy and whey by fourier transform infrared spectroscopy (FTIR). Journal of
Food Engineering, 214, 166–174. https://doi.org/10.1016/j.jfood​
proteins fall into the high-quality protein range (DIAAS = 75–99).
eng.2017.06.037
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observed in the protein quality lead to opportunities to enhance in high-protein canola meal, conventional canola meal, and soybean
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A. R. H., van Boekel, M. A. J. S., … Hendriks, W. H. (2013). The future
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AC K N OW L E D G M E N T S
Journal of Agricultural and Food Chemistry, 45(9), 3387–3394. https://
The authors thank Robin Spelbrink for his support and construc- doi.org/10.1021/jf970​070y
tive comments in completion of this manuscript. Our acknowledg- Carbonaro, M., Maselli, P., & Nucara, A. (2012). Relationship between
ments are also addressed to Michael Polhuis for proofreading this digestibility and secondary structure of raw and thermally treated
legume proteins: A Fourier transform infrared (FT-IR) spectroscopic
manuscript.
study. Amino Acids, 43(2), 911–921. https://doi.org/10.1007/s0072​
6-011-1151-4
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L.H., P.N., B.P., and M.C.L. are employees of Avebe U.A. D. (2012). Leucine supplementation chronically improves muscle
protein synthesis in older adults consuming the RDA for protein.
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ORCID org/10.1016/j.clnu.2012.01.005
Laure Herreman https://orcid.org/0000-0002-6609-7162 Cervantes-Pahm, S. K., Liu, Y., & Stein, H. H. (2014). Digestible indis-
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