Criteria and Significance of Dietary Protein
Sources in Humans
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The Protein Digestibility–Corrected Amino Acid Score1
Gertjan Schaafsma
Center of Expertise Nutrition, DMV International-Campina Melkunie, 6700 AA, Wageningen, the Netherlands
ABSTRACT The protein digestibility– corrected amino acid score (PDCAAS) has been adopted by FAO/WHO as
the preferred method for the measurement of the protein value in human nutrition. The method is based on
comparison of the concentration of the first limiting essential amino acid in the test protein with the concentration
of that amino acid in a reference (scoring) pattern. This scoring pattern is derived from the essential amino acid
requirements of the preschool-age child. The chemical score obtained in this way is corrected for true fecal
digestibility of the test protein. PDCAAS values higher than 100% are not accepted as such but are truncated to
100%. Although the principle of the PDCAAS method has been widely accepted, critical questions have been
raised in the scientific community about a number of issues. These questions relate to 1) the validity of the
preschool-age child amino acid requirement values, 2) the validity of correction for fecal instead of ileal digestibility
and 3) the truncation of PDCAAS values to 100%. At the time of the adoption of the PDCAAS method, only a few
studies had been performed on the amino acid requirements of the preschool-age child, and there is still a need
for validation of the scoring pattern. Also, the scoring pattern does not include conditionally indispensable amino
acids. These amino acids also contribute to the nutrition value of a protein. There is strong evidence that ileal, and
not fecal, digestibility is the right parameter for correction of the amino acid score. The use of fecal digestibility
overestimates the nutritional value of a protein, because amino acid nitrogen entering the colon is lost for protein
synthesis in the body and is, at least in part, excreted in urine as ammonia. The truncation of PDCAAS values to
100% can be defended only for the limited number of situations in which the protein is to be used as the sole
source of protein in the diet. For evaluation of the nutritional significance of proteins as part of mixed diets, the
truncated value should not be used. In those cases, a more detailed evaluation of the contribution of the protein
to the amino acid composition of the mixed diet is required. From such an evaluation, it appears that milk proteins
are superior to plant proteins in cereal-based diets. J. Nutr. 130: 1865S—1867S, 2000.
KEY WORDS: ● protein quality ● amino acid score ● scoring pattern ● digestibility ● critical evaluation
It is well accepted that the nutritional value of proteins may essential amino acid requirements of the preschool-age child as
differ substantially depending on their (essential) amino acid published in 1985 (FAO/WHO/UNU 1985) (Table 1). Sub-
composition and digestibility. For many years, bioassays, sequently, this percentage is corrected for the true fecal digest-
mainly with rats, were the methods of choice to assess the ibility of the test protein, as measured in a rat assay. This
nutritional value of proteins. This value was expressed in scoring method, known as the protein digestibility– corrected
parameters such as protein efficiency ratio, net protein utili- amino acid score (PDCAAS),2 was adopted as the preferred
zation and biological value. In 1989, a joint FAO/WHO method for measurement of the protein value in human nu-
Expert Consultation on Protein Quality Evaluation (FAO/ trition. Proteins with PDCAAS values exceeding 100% were
WHO 1990) concluded that protein quality could be assessed not considered to contribute additional benefit in humans and
adequately by expressing the content of the first limiting were truncated to 100%. The PDCAAS formula is shown
essential amino acid of the test protein as a percentage of the later.
content of the same amino acid in a reference pattern of
essential amino acids. This reference pattern was based on the PDCAAS共%兲
mg of limiting amino acid in 1 g of test protein
⫽
mg of same amino acid in 1 g of reference protein
1
Presented at the symposium “Criteria and Significance of Dietary Protein
Sources in Humans,” held in San Francisco, CA, on October 4, 1999. The ⫻ fecal true digestibility 共%兲 ⫻ 100
symposium was sponsored by the National Dairy Council; International Dairy
Federation; United Kingdom Dairy Association; Dairy Farmers of Canada; Davisco Table 2 shows values for protein efficiency ratio, true fecal
Foods International, Inc., New Zealand Milk; CAMPINA MELKUNIE, Zaltbommel,
The Netherlands; Land O’Lakes; and CERIN. Published as a supplement to The
Journal of Nutrition. Guest editors for this publication were Gregory D. Miller,
2
National Dairy Council, Rosemont, IL, and Daniel Tome, Institut National Abbreviation used: PDCAAS, protein digestibility– corrected amino acid
Agronomique, Paris, France. score.
0022-3166/00 $3.00 © 2000 American Society for Nutritional Sciences.
1865S
1866S SUPPLEMENT
TABLE 1 the essential amino acid requirement values (mg/kg body
weight/d) and this safe level of high quality protein intake
FAO/WHO/UNU amino acid requirement pattern based on (g/kg body weight/d), thus resulting in values of mg/g of
amino acid requirements of preschool-age child1 protein for each essential amino acid.
Although there is no evidence to reject the assumption that
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Amino acid Requirement both numerator and denominator of these ratios include sim-
mg/g crude protein
ilar margins of safety, this has not been validated. A difference
in safety margins of nominator and denominator would result
Isoleucine 28 in an incorrect reference pattern with underestimated or over-
Leucine 66 estimated values.
Lysine 58 Another issue is that the current reference pattern is re-
Total sulfur amino acids 25 stricted to the indispensable amino acids and does not include
Total aromatic amino acids 63
Threonine 34
amino acids that become indispensable under specific physio-
Tryptophan 11 logical or pathological conditions, such as cystine, tyrosine,
Valine 35 taurine, glycine, arginine, glutamine and proline. This implies
that these latter amino acids should also contribute to the
Total 320
nutritional value of a protein (van Hooydonk 1994).
1 From FAO/WHO/UNU Expert Consultation 1985. These considerations plead for a critical contemplation of
the current scoring pattern.
digestibility, amino acid score and nontruncated PDCAAS for Validity of true fecal digestibility correction
some selected proteins. As recognized by the FAO/WHO Expert Consultation on
Now, after ⬃10 y of experience with the PDCAAS protein quality evaluation (1990), the intestinal flow of amino
method, it can be concluded that the method has been acids beyond the terminal ileum is an important route for
adopted widely. On the other hand, critical questions have bacterial metabolic consumption of amino acids. Amino acids
been raised in the scientific community (Dutch Dairy Foun- that appear in the colon are most probably lost for body
dation on Nutrition and Health 1995, Darragh et al. 1998) protein synthesis. Therefore, ileal rather than fecal digestibil-
about the following three PDCAAS issues: 1) the validity of ity is the critical biologically relevant parameter for amino acid
the preschool-age child amino acid scoring pattern, 2) the or protein digestibility. The Expert Consultation recognized
validity of the true fecal digestibility correction and 3) the the shortcomings of the true fecal digestibility correction and
truncation of PDCAAS values to 100%. recommended methodological studies to resolve uncertainties
These issues are discussed later; it is concluded that it is about the contribution and variation of endogenous amino
timely to evaluate the PDCAAS method in its current form. acid losses at the terminal ileum before the determination of
ileal digestibility could be recommended to replace fecal di-
Validity of preschool-age child amino acid scoring pattern gestibility. Since then, several studies in this field were pub-
This reference scoring pattern (Table 1) is based on amino lished (e.g., Caine et al. 1997a and 1997b, Huisman et al.
acid balance studies performed ⬃20 y ago by Torun et al. 1993, Rowan et al. 1994, Van Leeuwen et al. 1996) indicating
(1981) and Pineda et al., 1981) in a limited number of 2-y-old that antinutritional factors associated with dietary proteins
children. These children were recovering from malnutrition may enhance substantially endogenous losses of amino acids
and thus not representing normal healthy preschool-age chil- and therefore decrease the nutritional value of the protein.
dren. The results of these studies, which so far have not yet Only true ileal digestibility of amino acids will take these losses
been published in peer-reviewed international journals, were into account (Darragh et al. 1998), and it is therefore timely
expressed in mg/kg of body weight/d and were assumed to to consider the use of ileal instead of fecal digestibility values.
include a safety margin of the same magnitude as that of the
FAO/WHO safe level of high quality protein (meat, fish, egg, Truncation of PDCAAS values to 100%
milk) intake for this particular group of children. The refer-
ence pattern was obtained by computing the ratios between According to the current PDCAAS method, values that are
higher than 100% are truncated to 100%, arguing that digest-
ible essential amino acid concentrations in a protein in excess
of those in the preschool-age child reference pattern do not
TABLE 2 provide additional nutritional benefit. This statement is cor-
True fecal digestibility, amino acid score and PDCAAS rect when the protein in question is the sole source of protein
in the human diet, as occurs in infant feeding practices and
for selected proteins1
under special conditions, like enteral feeding. However, under
Protein PER Digestibility AAS PDCAAS all other conditions, humans consume mixed diets with pro-
teins from a variety of sources. Under such conditions, the
% power of high quality proteins to balance the amino acid
pattern of the mixed diet is extremely relevant. A classic and
Egg 3.8 98 121 118 widely accepted example in this regard is the combination of
Cow’s milk 3.1 95 127 121 milk and wheat, in which the relatively high lysine concen-
Beef 2.9 98 94 92 tration of milk proteins compensates for the low concentration
Soy 2.1 95 96 91
Wheat 1.5 91 47 42 of this essential amino acid in wheat. So it can easily be
computed that 1.2 g of casein can balance 1 g of wheat protein,
1 Data from FAO/WHO Expert Consultation 1990, European Dairy whereas 6.2 g of soy protein would be needed to do so (Table
Association 1997, and Renner 1983. 3). The truncation of PDCAAS values thus largely eliminates
PROTEIN DIGESTIBILITY–CORRECTED AA SCORE 1867S
TABLE 3 (1997b) Endogenous recoveries of true ileal digestibilities of amino acids in
newly weaned piglets fed diets with protease-treated soybean meal. J. Anim.
Amount of protein needed to upgrade 1 g of wheat protein to Sci. 75: 2970 –2979.
Darragh, A. J., Schaafsma, G. and Moughan, P. J. (1998) Impact of amino acid
obtain the preschool-age child’s lysine requirement level of availability on the protein digestibility corrected amino acid score. Proceed-
58 mg/g mixed crude protein ings of the Nutrition Week of the International Dairy Federation, Wellington,
Downloaded from https://academic.oup.com/jn/article-abstract/130/7/1865S/4686203 by Library - Faculty of Medicine Ramathibodi Hospital user on 03 August 2020
New Zealand, March 9 –11, 1998.
Dutch Dairy Foundation on Nutrition and Health (1995) Proceedings of the
Protein Protein supplement needed International Workshop on Nutritional Aspects of Milk Proteins in Comparison
with Other Proteins, organized by the Dutch Foundation on Nutrition and
g Health, Utrecht, the Netherlands, March 13–14, 1995.
European Dairy Association (1997) Nutritional Quality of Proteins. European
Beef 1.0 Dairy Association, Brussels, Belgium.
Cow’s milk 1.6 FAO/WHO Expert Consultation (1990) Protein Quality Evaluation. Food and
Egg 2.6 Agricultural Organization of the United Nations, FAO Food and Nutrition Paper
Soy 6.2 51, Rome.
FAO/WHO/ÚNU Expert Consultation (1985) Energy and Protein Require-
ments. Technical Report Series 724. World Health Organization, Geneva.
Huisman, J., Verstegen, M.W.A., Van Leeuwen, P. & Tamminga, S. (1993)
Reduction of N pollution by decrease of the excretion of endogenous N in
pigs. In: Nitrogen Flow in Pig Production and Environmental Consequences,
the differences in the power of high quality proteins to balance pp. 55– 61. Pudoc Scientific Publishers, Wageningen, the Netherlands.
the amino acid composition of inferior proteins. This is highly Pineda, O., Torun, B., Viteri, F. E. & Arroyave, G. (1981) Protein quality in
relevant, not only for the low lysine content of cereals but also relation to estimates of essential amino acid requirements. In: Protein Quality
for the low content of S-containing amino acids and threonine in Humans (Bodwell, C. E., Adkins, J. S. & Hopkins, D. T., eds.), pp. 29 – 42.
AVI Publishing Company, Westport, CT.
of many plant protein sources. Thus, truncated PDCAAS Renner, E. (1983) Milk and Dairy Products in Human Nutrition. W-Gmbh
values do not provide information about the potency of a Volkswirtschaftlicher Verlag, München, pp. 90 –130.
protein to balance inferior proteins, and a solution for this Rowan, A. M., Moughan, P. J., Wilson, P. J., Maher, K. & Tasman-Jones, C.
problem should be found. (1994) Comparison of ileal and fecal digestibilities of dietary amino acids in
adult humans and evaluation of the pig as a model for animal digestion
The questions about the validity of the amino acid scoring studies in man. Br. J. Nutr. 71: 29 – 42.
pattern and the application of the true fecal rather than the Torun, B., Pineda, O., Viteri, F. E. & Arroyave, G. (1981) Use of amino acid
true ileal digestibility correction as well as the truncation of composition data to predict protein nutritive value for children with specific
PDCAAS values warrant a critical evaluation of PDCAAS in reference to new estimates of their essential amino acid requirements. In:
Protein Quality in Humans (Bodwell, C. E., Adkins, J. S. & Hopkins, D. T.,
its current form as a measure of protein quality in human diets. eds.), pp. 374 –393. AVI Publishing Company, Westport, CT.
Van Hooydonk, A.C.M. (1994) Definition of the nutritional value of dietary
LITERATURE CITED proteins. In: Protein Definition. Proceedings of the 1st IDF Symposium, Min-
neapolis, MN, October 1993. International Dairy Federation, Brussels.
Caine, W. R., Sauer, W. C., Tamminga, S., Verstegen, M.W.A. & Schulze, H. Van Leeuwen, P., Veldman, A., Boisen, S., Deuring, K., Kempen, G.J.M., Derksen,
(1997a) Apparent ileal digestibilities of amino acids in newly weaned piglets G. B., Verstegen, M.W.A. & Schaafsma, G. (1996) Apparent ileal dry matter
and fed diets with protease-treated soybean meal. J. Anim. Sci. 75: 2962– and crude protein digestibilty of rations fed to pigs and determined with the
2969. use of chromium oxide (Cr2O3) and acid-insoluble ash as digestive markers.
Caine, W. R., Tamminga, S., Verstegen, M.W.A., Sauer, W. C. & Schulze H. Br. J. Nutr. 76: 551–562.