Anda di halaman 1dari 10

Plant proteins in relation to human and amino acid nutrition12

Vernon ABSTRACT
capita North supply American

protein

R Young

and Plant

Peter
protein on

L Pellett
foods a worldwide sources contribute basis of 65% and 32% are ofthe in discussed per the generally fruits, most and important oil-seed divided nuts. In groups legumes. into the cereals, context are cereal vegetables of human grains (including protein and food legumes), nutrition, legumes, the in-

of protein region.

These

protein

in relation
quirements, teins acids review

to their
and

amino

acid
protein

content,
quality.

human
Mixtures

amino
of

acid
plant

repro-

cluding

dietary

The
or animal

world

supplies
are

of protein
difficult

that

are derived
but

from
their

either
approximate

plant

can
for

serve
meeting ends

as a complete
human a list of with

and
physiological a series

well-balanced
requirements. of myths

source
and realities

of amino
This short con-

sources

to estimate,

amounts

are given

in Table supply
for

1. On a global
of edible protein. portion

basis,
The of the

plants
cereal worlds

provide
grains, food

Downloaded from ajcn.nutrition.org by guest on March 24, 2014

cerning
tion and professional

the relationship
a list of some and informed l203S-

between
nutritional

plant
issues consumer.

protein

and Am J

human
to the

nutrihealth

65% of the world in particular. account


protein

a substantial

of concern

(Table 35% there


from

2) and energy. of the are


animal and

On the other capita discrepancies

hand, in per
between

animal of food capita


the

products protein. protein in North protein. of the mdiStates, developed

C/in

Nuir

contribute However,
supplies

per

availability
sources

1994;59(suppl):

l2S.

marked (Table

protein

KEY
mentation, score,

WORDS
nutritional timing,

Amino
digestibility,

acids,
limiting

requirements.
nitrogen, amino balance, acid,

protein,
amino lysine

compleacid

and

developing

regions

I ; ref 6). For

example.

quality,

America whereas Far


viduals

animal products supply 70% of the food the equivalent figure is 20% for the populations and
in rural

East,

may
areas

approach
of India

much
and

lower
Indonesia.

levels
In the

for that

many the
as

United

Introduction Plants
constitute tein, essential

food are the predominant


a primary fatty It is not resource acids, and

consumption
made by plant

survey
protein groups

data
and

(Table
for the

3) show
daily population

contriintake

harvesters
of carbon, utilizable therefore, household

of solar
vitamins, energy that with the

energy
minerals, for plant bulk

and

they
profood have

bution

to the

estimated

protein

is 30% for all age Also shown in Table


(essential) tryptophan, amino which acids

a whole.

3 is the pattern
lysine. sulfur across is constant

ofintake
amino all age

ofthe
acids, groups.

indispensable
threonine, and

human foods of its

production. always supplied

surprising, global

the

food

energy been
century that have

intake major
we

and players
it will is be

most

of its protein the


that directly market

needs. course
before or

Indeed, of human
the turn crop by

plants history
of the

have ( 1).
next

in shaping
anticipated using, to

In part because livestock of the energy and available

production involves protein of plants that

a potential loss could otherwise

Furthermore,
been

indirectly,

products addition,

be used to meet human needs, it has been a popular view, and one that was echoed at the Second International Congress on Vegetarian Nutrition, to recommend significant reductions in the
amounts their direct of cereals use as and foods legumes for humans. used for feed and to the increase potential Furthermore,

tailored

specifications

the

deletion,
derstanding responsible nutritional fective of plant

or modification
of for value manipulation foods the genetic encoding of grains, (4). in Western-type

of genes
organization seed for storage

(2, 3). With


and proteins will an has

an increased
of it is likely be amenable contribution that

ungenes the

regulation

health

benefits

of this

shift

in the

composition

of human

diets

example,

to ef-

have received considerable attention in recent years and this topic was also a major focus of interest at the Congress. Therefore, the nutritional aspects
of diets

Additionally, diets

increased been

of plant
based mainly

foods
on

and
plant

the protein
sources

nutritional
deserve our

adcon-

recommended

as a

way

to reduce

the

risk

of chronic
in brief,

diseases
the role

(5).

For

these
food

reasons
proteins

equacy sideration.

it is pertinent in human

to consider, nutrition.

of plant

To assess needs

the nutritional subjects

role under

of plant various

proteins conditions

in meeting we should

the first

of human

Quantitative Throughout
cies for food

importance history,
and at

of major humans have species most

plant used have plant


Printed

crops
tion,

From

the Clinical
of and the

Research
Department

Center
Massachusetts of

and Laboratory
Institute Human Nutrition,

of Human
of University

Nutriof

School

Science,

Technology,

some been

3000

plant

spefor are
1994

Cambridge, Massachusetts
2

least

I 50

cultivated population which

at Amherst.

commercial depends
Am J Cli,z

purposes. on
Nutr

However,

of the worlds crops,


in USA.

Reprints

not available.
Institute

Address

correspondence
Cambridge,

to VR Young,
MA 02142.

EI8-

approximately

20 different

613,

Massachusetts

of Technology.

1994:59(suppl):1203S-l2S.

American

Society

for

Clinical

Nutrition

I 2035

12045 TABLE
Energy

YOUNG

AND

PELLETT

1
and protein supplies per capita per day for selected geographic

TABLE
Protein

3 consumption and amino acid pattern for various age groups

and economic

regions

for 1989
Animal protein
g

(female)
Total protein Plant protein

in the United

States
Proteins Amino acids2

Energy
kca! (Mi)

Carbohydrate
%

Total
Age group protein Plant

Meat,

poultry.
fish

Grain
products Ly Saa
Png/g

Thr protein 40 40 39 39 38

Try

Region Developing Far East Middle East Africa Latin America Economic class
Least developed

2846 2450 2954 2363

(11.91) (10.25) (12.34) (9.89)

73 75 67 72

14 II 17 12

61 59 78 58

77 81 78 79 <I 6-8y 19-22y 35-50y >75 y y

gid 42
68 65 65 59

gld 27
33 30 29 32

55
154 183 191 48

59 227 184 169 190

69
69 72 71 68

31 35 35 34 34

12 12 12 12 12

2732(11.43) 2058 2409 3417 3457 3650 3240 (8.61)

65
76 74 53 51 48 50 67

29
9 11 61 60 73 66 25

68
52 58
104

57
83 81 42 42 34 33 65

Low income Developed Western Europe North America Oceania World

(10.08)
(14.30) (14.46) (15.27) (13.56)

Based
Ly.

on US Department
lysine: Saa, sulfur amino

of Agriculture acids: Thr.

Food threonine:

Consumption Try.

Data tryptophan.

(reference

7).
2

103 110 98 71

2710(11.34)

Based

on FAO/Agrostat

data

(reference

6).

The nents: amino

requirement for dietary protein consists 1) the requirement for the nutritionally acids
and for

of two compoindispensable lysine, methionine, under


acids

Downloaded from ajcn.nutrition.org by guest on March 24, 2014

(histidine, threonine,
conditionally

isoleucine, tryptophan,

leucine, and

phenylalanine, turn tein


This

valine)
amino

all con(cystine,

our

attention and
has

to the estimates for the


reviewed

of requirements indispensable
us (8, 9) and by

for total amino


others (10,

proacids.
1 1)

ditions

indispensable

(nitrogen)
subject

specific

been

tyrosinc, specific

taurine, physiological

glycine, and

arginine, pathological

glutamine, conditions

proline) under and 2) the re-

and
issues

so an abbreviated
relevant to plant

account
proteins

of some
will be

of the
presented

more
here.

important

Protein quality
The joint

and amino considerations


requirements of humans, of the Food panel

acid

requirements

and

protein

quirement for nonspecific nitrogen for the synthesis of the nutritionally dispensable amino acids (aspartic acid, asparagine, glutamic acid, alanine, serine) and other physiologically important nitrogen-containing compounds such as nucleic acids, creatine, and porphyrins. accepted that With respect to the first component, it is usually the nutritive values of various food protein sources extent individual which
adequate

for total were and

protein, reviewed Agriculture

at various and evaluated

stages

during recently

the by a

are to a large ability efficiency


in support

determined a given
state

by the source

concentration amino of food acids. protein


health

and Hence,
depends

availthe
both

life cycle

of the with

indispensable
of nutritional

Organization,

the World (FAO/

is utilized

Health Organization, and the United Nations University WHO/UNO) (1 1). In Table 4, the safe intakes of high proteins, from These trogen they eggs, data reveal defined meat, were in the FAOIWHO/UNU given from (1 1) report for different growth and and milk, are derived largely studies an age-related of adequate and, when decline protein

of an

quality
as those TABLE 4 Safe protein Age group intakes as proposed in 1985 by FAO/WHO/UNU Males gprotein 3-6mo 6-9mo 1.85 1.65
1.50 1.20
y 1.15

age groups. metabolic niweight, needs for

balance

expressed in dietary nutritional

per kg body protein status.

Females2
. kg . d

maintenance

1.85 1.65
1.50 1.20
1.15

TABLE

9-l2mo

Relative
capita

importance
intake for

of various
1989

food groups

in average

world

daily

per

l-2y
2-3

3-Sy

1.10 1.00

Energy kcal(kJ) Total plant Cereals Pulses, nuts, oil crops Starchy roots Other vegetables Fruits Total animal
Total

Percent of energy % 84 51
4 5

Protein
g

Percent of protein
%

1.10

S-7y 7-lOy l0-12y 12-14y 14-l6y

1.00 1.00 1.00


0.94

1.00 1.00 1.00


0.95 0.90

2277 (9 526) 1385 (5 794)


109 (456)

46. 1 33.7
6.0 2.0

65 47
8 3

l6-l8y Adults

0.88 0.75

0.80 0.75

141 (590) 46 ( 192)


65 (272)

2
2

2.5
0.8

4
1

433 (1 811)
2710(11339)

16
100

25.0
71.1

35
100

Based

on FAO/Agrostat

data (reference

6).

Adapted from reference 1 1 . Values are uncorrected for nutritional value (amino acid scores) of mixed dietary proteins for infants and children and digestibility for all groups. 2 Safe protein intakes for pregnant females, intakes in table + 6g: for lactating females (0-6 mo), intakes in table + 17.5 g; and for lactating females (6 mo), intakes in table + 13 g.

PLANT on the
acids

PROTEINS TABLE Survey S of the amino

12055

physiological
and total nitrogen

requirements
and on

for
the

the

indispensable
of

amino
specific

concentration

acid content

of different
Sulfur

food protein

sources

amino
This

acids
raises

in the source
the question

of interest.
of the content and balance of indis-

Food

source

Lysine

amino

acids
mg/g

Threonine
protein

Tryptophan

pensable

amino data

acids

in plant amino

and acid

animal

protein

foods. of foods

There (12,
Legumes Cereals Nuts, seeds
Fruits

are extensive

on the summary sources the most

composition

13). For present in different food are likely to be shown, the much lower than
acids are

purposes, Table 5 gives the amounts of those indispensable amino acids that limiting amino acid in all major In addition,
in legumes

in plant

protein

foods.

As

10 10 45 14
64 31
45

25 37

3
S

38 3 32 4 36 3 29 7

12 4 12 2 17 3
11

indispensable concentration foods.


lower

lysine is consistently plant-food protein sulfur-containing


fruits and and

at a groups amino
is

12

Animal

foods

85

46 17 27 6 38

44

12

in animal
distinctly

the amounts survey


various

threonine

lower animal
acid

in cereals origin.
and the amino

compared A more
acid score

with extensive
for

found of the
plant

in proteins limiting
protein

of
is

1 SD. Based on data from FAO (reference of Agriculture (reference 13).

12) and US Department

amino
foods

presented Given and tional protein tional review). protein official cedure comparative animal

in Table these significance nutrition. quality. One efficiency use since does not proteins.

6. of amino relevant acid content about needs used (see the been proteins procedure has been satisfactorily among their plant nutrinutrithe the and pro15 for it is now in reference Hence, to ask the topic have of food rat bioassay which predict

The quirements

1985

FAOIWHOIUNU in various age groups

estimates and in Table in Table

of the the estimates

amino

acid

reby

comparisons

proposed

to meeting

of human to assess ref termed this

US authorities (10) are shown purposes, if the values given essential adults would amino acids were adopted, be overestimated.

7. For amino acid scoring 7 for the concentration of

Downloaded from ajcn.nutrition.org by guest on March 24, 2014

we introduce approaches value is the (PER),

of protein

in relation the nutritional In contrast,

to the

total

protein

needs for children child pattern

of

Various nutritional example ratio

value of a protein adoption ofthe

in widespread the nutritional

would underestimate the value When the FAO/WHOIUNU


timates for the adult, which
(see

of a protein (1 1) amino
are expressed

for adults. acid requirement


per unit of protein

esacid
be

first proposed necessarily

in I 9 19 ( 1 6). However,

need,
pattern

are

compared

Tables
and animal

5 and
protein

7) with
sources,

the food

amino
it should

value of all plant protein foods intended for direct sumption (1 7, 18). This is particularly so for legume
proteins. Alternative procedures that would be more

human conand oil-seed


directly ap-

of various

plant

evident much
ids,

that higher

the amounts (per


proteins

of amino of protein) acids,


lysine

acids than including

in these required.
proteins

sources amino
predicted

is all acto

unit
and

As a result,
are

plicable

to human

protein

and

amino

acid

nutrition FAO/WHO

have

been Expert on the re-

of the indispensable
in soy

amino

the sulfur

proposed and developed. The procedure that was adopted Consultation concept in I 946 lationship tent
as the

in cereal

by a recent evaluation concept who amino


acid

( 19) on protein of an amino by Block between limiting acid and score. Mitchell

quality This (20), value The

is based was

first introduced a linear and score


food

observed acid

be in considerable excess of adult needs. Thus, all usual food proteins would readily meet and even exceed the requirement for the indispensable amino acids, providing that the dietary protein supply was equal to or above the safe protein intakes (Table 4). On reason tional cluded
fants,

the biological amino


of the

of proteins
in the

the conis defined


protein

of their

acid.
limiting

the above basis it would to be further concerned quality of plant proteins that our attention should
particularly because they

be concluded that with an assessment

there is little of the nutribe conand inprotein formula, there is


FAOIWHO/ for most in-

concentration

amino

and tion amino portant pattern lating


teins

is expressed of the acid issue an amino


of interest.

as a proportion limiting (15). the score the amino It was for amino Hence, choice

or percentage acid a particularly of the nutritional protein


Mitchell and

of the concentraor reference critical acid quality


(20)

in adults. It could also be focused on children


might be given diets

containing

same pattern

in a standard amino

a single imsources, possibly


increasing UNU

food

protein

source infants with


that the (10)

or

a limited

number

of

and reference

becomes acid
When

for example, supplemented


evidence (I I) and national

fed a diet of a proprietary strained foods. However,


current requirement international estimates

to be used

for assessing
Block

or for calcuof prothis proposed

for a food acid later human


acid amino

or mixture of egg that


in egg

dispensable Several evidence, groups

amino which
for roles the of

acids would

in adults are seeking strengthen


to be and

are

far

too

low

(9,

23,

24). this of imasin

scoring was
high

procedure,
amounts of

composition determined
acids

proteins
un-

(25-27)

to further the case and would


taken

substantiate have
protein

used

as a standard. many scoring feature 1985, before protein amino published that only infants 15% proteins
of human

the relatively
proteins

for the inadequacy important


sources to comprehensively

indispensable

the international
plications sess the

recommendations
approaches both plant

dervalued
use

nutrition,
requirements

which

led

to the
for

of estimates

amino

as a basis

animal

food

subsequent A common proposed ergy and reference despite showed the form needed

systems of most when

(1 1, 21, 22). of the amino was published, was used for requirement of their acids whereas w35% amino (1 1, 22). acid scoring report was studies data total systems on enthe FAO/WHOIUNU

human The quirements from

nutrition. specifics were recent more of this previously data new research reviewed arrived on human at a new, amino tentative acid However, set of reby us (9, 23, 24).

requirements acid pattern amino needed or less acid

that a single on all ages, that generally acids apparently in

we have

estimates for the amino shown in Table 8, and made by FAO/WHO/UNU

acid needs of adults. These values are are compared with the I 985 estimates for the children aged 2-5 y. slightly similar threonine and pattern is quite

amino adults

of indispensable

It can be seen that, except for a lower lower lysine content, our proposed adult

1206S
TABLE 6

YOUNG

AND

PELLEU TABLE 6 (Continued)


LAA score Lysine

Protein concentration, limiting score for selected plant foods

amino

acid (LAA)

score

and lysine Protein (amino acid) score

LAA

Protein % Cereals Amaranth Barley Buckwheat Bulgur Corn Millet Oats Rice brown Rice white Rye Sorghum Triticale Wheat hard Wheat durum Wheat flour Spaghetti
Legumes

(amino

score acid)

Lysine score Vegetables Turnip Yam Fruits Apples


Avocados

% (continued) 0.9
1.5

53 (Aaa) 66(Lys) 75 (Aaa)


82 (Lys)

69 66 109
82

14.5 12.5 13.3


12.2

89 (Lys)
64 (Lys)

89
64

0.2
2.0

87 (Lys)

87
48

9.4 11.0 16.9 7.9 7.1 14.8 11.3 13.2 12.6 13.7 10.3
12.8

48 (Lys) 49 (Lys) 33 (Lys)


72 (Lys) 66 (Lys)

49 33
72

66
62 62

62 (Lys)

71 35 48 46 38 38 33
100 100 100 100

(Lys) (Lys) (Lys) (Lys) (Lys) (Lys) (Lys)

Bananas Figs Orange Peach Pear Pineapple Plantain Plum

1 .0 0.8 0.9
0.7

80 (Lys) 67 (Leu, 37 (Leu)


57 (Lys)

Lys)

80 69 86
57

0.4 0.4
1.3 0.8

62 (Lys) 74 (Leu)
69 (Leu) 37 (Lys)

62 111
80 37

35 48 46 38 38 33 118 118 115 117 120 116 92 120


62

Lys, lysine; Saa, sulfur amino acids; Leu, leucine; amino acids. Based on FAO/WHOIUNU data (reference ences 12, 13, and 14.

Aaa, aromatic 1 1) and refer-

Downloaded from ajcn.nutrition.org by guest on March 24, 2014

to the 21.9 23.6 19.3 23.5


28.1 school

pattern and

recommended

by

FAOIWHOIUNU
(2-S y). If

(1 1) for
these

preas we the

Bean white Bean kidney Chick peak Cow pea Lentil Lima bean Lupine Mungbean Peanut Pigeon pea Soybean Wing bean Nuts and Seeds Almond Brazil Cashew Coconut Pecan Pistachio Walnut
Cottonseed

estimates believe

early school-age children of amino acid requirements are for reasons discussed

revised

in adults elsewhere

are rational,

they

(9, 23, 24),

21.5 36.2 23.9


25.8 21.7 36.5

86 (Saa) 95 (Saa)
78 (Saa)

nutritional value of different protein sources would not be affected as markedly by the age of the consumer. This is in contrast to the position adopted in the 1985 FAO/WHO/UNU report. Based are protein ommend The first position on the revised given in Table quality estimations 8, it follows nutrition of amino that for
it is

83 (Saa) 62 (Lys) 91 (Saa)


100 100

acid
only

requirements of
necessary to

that dietary
rec-

evaluation

29.7 20.4 14.3


15.3

121 115 124


58
65

in human

use of two amino acid requirement, pattern would be that for the infant,
(1 1) should be based on

or scoring, patterns. which according to


the amino acid com-

FAO/WHO/UNU

58 (Lys)
65 (Lys)

of breast

milk;

the second,

as shown for made which


for 2 y of

in Table ages
age.

8, would y, which
view is

3.3 8.0 14.9 14.3 41.0


24.5

92 (Lys) 76 (Lys) 65 (Lys)


100

92 76
65

be the amino acid requirement would be applied to all groups now reflected by in the recommendations FAO/WHO
amino

pattern above

2-5
This

by the expert that


the group

group 1985
2aged

47 (Lys) 88 (Lys)
100

seed Sesame seed Sunflower seed Vegetables Bean (green) Broccoli Cabbage Carrots
Pumpkin Cassava

107 47 88 129
55

convened
FAO/WHOIUNU 5 y be used

(19),
acid

proposed of foods adults. purposes, acid score

the

requirement

to assess

the protein

quality

in reference the so-called (PDCAAS),

to

17.7
22.8

55 (Lys) 71 (Lys) 83 (Lys) 67 (Leu)


73 (Saa) 58 (Saa)

young children, FAO/WHO protein which

older children, (19) proposed,

and also for scoring amino

71 83
82

digestibility-corrected can be defined as follows: Amino acid content

1.8 3.0
1.2 1.0

81 67
56

PDCAAS

Amino

(mg/g

Okra Onion Peas (green) Pepper sweet Potato Spinach Squash Sweet potato Taro Tomato

1.3 2.0
1.2 5.4

44 (Leu) 70 (Lys)
53(Leu) 85 (Saa)

acid content FAO/WHO/UNU digestibility

protein)

in food

in 1985 pattern

protein

x digestibility for ages in this 2-5 y acid of to

70
82 101

It should scoring

be noted procedure,

that

is included

amino

to allow

for differences

in the digestibility specifically

0.9
2.1 2.9 1.2 1.7
1.5

77 (Lys,
91 (L.eu) 100 70(Thr) 85 (Lys)

Leu)

77

105 105 95 85
77
64

the different the digestibility

food-protein of plant

sources. We will refer protein foods below.

Amino
The

acid score
amino acid

and plant
scoring procedure

protein
appears

quality
likely to be adopted for food protein

0.9

77(Lys) 56 (Leu)

by the US government

as the official

procedure

PLANT TABLE
Estimates

PROTEINS

12075

7
of amino acid requirements of preschool children, older children, and adults

Intake Preschool
Amino acid (2-S y) mg Histidine Isoleucine Leucine

for wt Adults
(

Intake Preschool
(2-S y)

by protein Adults
( 18 y)

Schoolchildren2
(10-12 kg body
-

Schoolchildren2
(10-12 mg/g protein
-

y) wt d

18 y)

y)

8-12 10.0

28

16
28 13

31.0 73.0

28.0

Lysine
Methionine and cystine

64.0
27.0

44.0 44.0
22.0

14.0
12.0 13.0

66
58 25

44
44 22

19
16 17

Phenylalanine
Threonine

and tyrosine

69.0
37.0

22.0
28.0

14.0
7.0

63
34

22
28

19
9

Tryptophan Valine Total (-histidine)


2

12.5 38.0 352.0

3.3 25.0 216.0

3.5 10.0 84.0

11 35 320

9 25 216

5 13 1 11

Adapted from reference 1 1. Based on NRC data (reference

10).

Downloaded from ajcn.nutrition.org by guest on March 24, 2014

quality evaluation and quality control we have argued in favor of this policy to briefly compare some based on the PDCAAS. In Table 9 we compare human the

of protein foods. Because (28) it might be worthwhile data with predictions of comthe the
of

tern for children aged 2-5 y is set too high then this would give the protein a lower numerical value for the score than would be obtained via a feeding-metabolic study. Because lysine is most likely to be the first limiting amino predominantly on cereal grains (30) more accurately the lysine content acid in addition requirement pattern. The reference amino PDCAAS protein a high and are the predicts products, nutritional concluded sole or major that acid in diets it is important of the reference to that are based to determine amino arrive at acid the soy

metabolic amino acid and The


variety

composition

mon hybrid and high-lysine PDCAAS for these different


nutritional value of the

maize cultivars.

have calculated prediction is that


is superior to that

high-lysine

pattern

used

the hybrid
in children,

maize normal

and this maize

has been
by

confirmed
(29).

in metabolic
A lower

studies
biological

to cereals,

well-processed

as summarized

Bressani

value

for

compared

with

two

varieties

of high-

such as isolated soy proteins value. We have reviewed that soy flour and soy source of protein

( 1 8), would have this topic in detail isolates, when they adeof cxcontaining

lysine maize was also reported (29). However, whether any significance should be given to the difference between the value for the score of 0.63 value studies the scores of the (Table of the 9) and high-lysine the numerical maize estimates as derived for from the the biological metabolic between content

have

in diets

quate energy and other essential nutrients, are fully capable promoting adequate growth in young infants (17, 18). For ample, Torun (3 1) gave graded amounts of one of two

is difficult to judge. and the metabolically and high-lysine maizes

The relative differences derived, biological valare small. acid If the lysine reference pat-

soy-pro-

ucs for the hybrid

FAOIWHOIUNU

(1 1) amino

TABLE 9 Indispensable
high-lysine

amino
maize

acid content

and amino

acid score

of normal

and

TABLE
New, corresponding

8
tentative amino acid requirement pattern estimates for preschool for adults children Highand Maize 1991 FAOIWHO
pattern2 Normal High-lysine

Amino

acid score

requirement

Amino

acid

Adult tentative requirement


mg kg d

Adult amino acid pattern2


mglg protein

Preschool child amino acid pattern2


Lysine mg/g protein

Amino

acid

Normal

lysine

mg/g N
177 206 827 256 193 507

mg/g N
363 175 413 0.44 >2.00 >1.00
> >

0.63 0.98 >1.00

Isoleucine

Isoleucine Leucine
Lysine

23 40
30

35 65
50

28 66
58

Leucine Sulfur amino


Aromatic

acids
acids

1 88
505 213

188
502
199

156
394 213 68

amino

I .00 I .00
0.89

>1.00
> I .00

Sulfur amino acids Aromatic amino acids


Threonine

I3 39
IS

25 65
25

25 63
34

Threonine Tryptophan Valine


Leucine-Isoleucine

0.83
> I .00 >1.00 >1.00

35 292
4.01

78

>

I .00

298
2.63

219
2.36

>1.00 >1.00

Tryptophan Valine

6 20 23.

10 35

11 35

Adapted Adapted
Corrected

from reference from reference


for digestibility,

29. 19.
assuming a value of 0.89 relative to ref-

Based on data from reference Adapted from reference 1 1.

erence

proteins.

l208S
tein isolates to children who had recovered from earlier

YOUNG
protein-

AND

PELLETT and indispensable amino acids that they contain. The concentra-

energy malnutrition with those obtained tation of the depending isolated soy

and using protein specific

compared nitrogen-balance milk as the reference protein. data tested criterion showed was used 86107% that

responses Interprevalue of milk, Hence,

of the nitrogen-balance on the

that the nutritive for comparison.

tion of protein and the quality of the protein in some foods of vegetable origin may be too low to make them adequate, sole sources of proteins when consumed in their traditional manner,
particularly for infants and children. However, children can

the protein nutritional value of the well-processed isolated soy proteins so far examined in young children is essentially cquivalent to that of milk protein. quality of specific soybeen reviewed previously Results of studies on the nutritional protein products in adults have also ( I 7, 1 8). In summary. the protein (Supro-620, Ralston an analysis adults, digestibility comparable of the > 80% of the

thrive on as well as recover from well-formulated diets based entirely plant foods, supply the quate health Mixtures

severe malnutrition if given on plant food sources. Thus, are able to of adehigh

in appropriate amounts and combinations essential nutrients required for maintenance and function. of plant protein For example. amino acids, grains proteins, foods may be

of potentially

nutritional value of an isolated soy Purina Co. St. Louis, MO), based on data, value was high high protein. (97%) for healthy The and true was of egg

nutritional quality. sulfur-containing flour, cates and that cereal oil-seed

although cottonseed, mainly

the soybean is low in peanut and sesame in lysine. This mdisoy protein. can be used

nitrogen-balance nutritional

are deficient in particular,

of the soy isolate was also with that for egg proteins. from the observation
in children

effectively in combination overall quality of the total protein, relatively tional greater This pertinent which good

with most cereal grains to improve the protein intake. A combination of soy a cereal that acids results the contains a in a nutrimixture is

Of particular importance metabolic studies, was the


this soy isolate when tested

findings in these that the protein


and adults was

various value of
consid-

is high in lysine, with concentration of s-amino

erably carried

higher out

than

what

would growing

be predicted rats. quality The of the

from latter soy

the PER assay isolate

assay

complementation; the protein quality of than that for either protein source alone. concept of protein, or amino of plant foods. acid, to a discussion Various

Downloaded from ajcn.nutrition.org by guest on March 24, 2014

in rapidly

seriously for chil-

complementation nutritional

is re-

underestimates dren and human view proteins man


tritional

the nutritional

adults. Perhaps the discrepancy between rat and data also explains why there appears to be a lingering by some professionals quality. reveal the emerges 1 8), Clearly that they of the From our as well the can as consumers more be and for recent, that direct soy hunusupthose of is of poor data

sponses are observed when two dietary proteins These have been classified by Bressani et al (33) types (Types I, II, III, and IV) as shown Type I is an example where no protein
is achieved. For example, this occurs with

are combined. into one of four effect


of pea-

held arc

in Figure 1. complementary
combinations

metabolic
value.

are of high methioninc and

Parenthetically, plementation others ( 17,

question here.

need own

studies of soy

methionine

supplementation

proteins

PROTEIN COMPLEMENTATION
Type I Type if

clearly unnecessary in adults. Soy proteins, or concentrates, are excellent sole sources and all amino acid needs when consumed portant intakes of total protein. Methionine soy-based the
soy protein

consumed as isolates for meeting nitrogen at physiologically imsupplementation of be desirable, although

infant
appears

formulas addition

may,

however,

methioninc

required to achieve high utilization of modest ( 1 8, 32) and is considerably lower from rat PER since the 1957
(2 1 ), who

than would have been predicted More than 30 y have passed FAO tritional ments. of amino that has data respect protein acid, value Provided requirements scoring of proteins that proteins (or or amino

assay report

data. of the the

first nu-

A. Pssmt
.14

B. Corn
I
I I I

committee as an official for meeting the availability an adjustment

selected

protein,

basis human is made

for assessing nutritional of the

0
0

require-

for the digestibility indispensable

ingested

Type III

Type .&

acids in the protein), the the concept of a desirable a great advantage acid can and content of the on the amino to evaluation

conclusion made by this group pattern of essential amino acid with foods range quality such and a pattern, food comwith and of

by comparison, of individual for a wide nutritional

binations

be appraised

of situations, of the diet

methods of improving it remains valid. In addition, the recent recommendations made by FAOIWHO ( 19) are entirely consistent with this view.

A. Corn B. Soy Flour

A. Soy Protein

B. Beef Protein
I 40 I 20

A.1008O

I 60

0
100

10080 0

60 40

40 60

20 80

0 100

B. 0
Additional
Complementation

20

40

60

80

20

issues
and timing of ingestion of proteins

% PROTEIN DISTRIBUTION IN DIET


FIG products of proteins of
logical sources.

1 . Four
value Adapted

types or protein from

of response, quality, reference

assessed arising 33. from

in terms mixing

of an of two

index food

of bioprotein

Important vegetable and

differences animal

among origin are

and the

between concentrations

food

PLANT TABLE
Digestibilities

PROTEINS of the need to ingest a significant amount of protein at each

12095 meal, or

10
of different sources of food protein in humans

or whether relative proteins % to

it is sufficient

to consume

protein

in variable daily intake intakes.

amounts meets

True digestibility % Reference


Egg Milk, cheese

Digestibility reference

at different meals as long exceeds the recommended According quirements

as the average or safe protein needs

to FAO/WHOIUNU refer to metabolic

(1 1), estimates that persist

of protein reover moderate

proteins
97#{247}32

100
3 3

periods of time. are conventionally implication day. Therefore, that

Although protein and amino acid requirements expressed as daily rates (of intake) there is no these amounts must be consumed at least of each physiological each and every that daily amino it is it is not essential, in adults,

Meat, fish Plant proteins Maize Polished rice Whole wheat Oatmeal Beans Maize, beans Indian rice diet
Brazilian mixed diet

94
95

100
100

856 88 4 86 5 86 7 78 78 77
78

89
93

intakes of protein, or presumably acid, must equal or exceed the apparently to achieve tenance There definitive
mentary

indispensable requirement;

90
90

sufficient for the average this level. This pattern of an adequate is a limited conclusion
proteins

intake over a number of days of intake would allow mainstate. to make of complefor pro-

protein

nutritional

82 82 81
82

database that on the timing


L-amino

we can consult of consumption


acid supplements

or of specific

Filipino mixed diet US mixed diet


1

88 96 1 1.

93
100

teins

that

are deficient

in one

or more

amino

acids.

Earlier

work

in rapidly growing tation of a protein

rats suggested with its limiting

that delaying amino acid

the supplemenreduces the value of feeding affects the

Downloaded from ajcn.nutrition.org by guest on March 24, 2014

2#{247}

Adapted from SD.

reference

of the supplement (35-38). of diets supplemented with

Similarly, the frequency lysine in growing pigs

overall efficiency of utilization of dietary protein (39, 40). There are few data available from human studies to assess the signifinut and and corn, where each similar of the protein lysine deficiency sources and have a common also decance studies of these can findings. However, in view characteristics with human that overall the meals daily (42). less protein However, of Phaseolus when and conditions D Wilson, of healthy proteins the relevance of rat and different metabolism Our studies utilization distributed efgiven commuit is not time at to a maizewas personal living pig quantitatively are both be questioned of the profoundly

ficient in other amino acids. Type II response combinations are made of two protein sources limiting amino and cottonseed cottonseed The third plementary overall of the best of response

is observed when that have the same

acid, but in quantitatively different amounts. Corn flour, for example, are both limiting in lysine but less inadequate than is corn. a true comeffect on the quality (Type III) demonstrates there is a synergistic mixture;

qualitative and quantative in rats and pigs compared in human adults showed was among fect bean
intervals

of protein subjects (41). dietary protein intake was

similar
two

whether or three was

is relatively

the supplementary vulgaris

type of response effect because value

in children diet
of > 6

of the addition somewhat

the supplement

nutritive

of the protein

the protein

h (R Bressani
for usual

mix exceeds that of each component alone. This type occurs when one of the protein sources has a con-

nication, 1992). We believe that necessary and to consume

siderably higher concentration of the most limiting amino acid in the other protein. An example of this response, based on studies in children (33), is observed when corn and soy flour are mixed so that from the
have

complementary

at the same

that separation of the proteins among of a day would still permit the nutritional mentation. tention. Because a diet and pool lysine. chronic, based relevance The size There lysine that are also is most in the physiological likely skeletal space pool of lysine serum may

meals over the course benefits of compledata to support amino this conin

60%

of the protein protein. IV response


amino

intake

comes

from when
The

corn both
protein

and

the

remainder Finally,
sources

soya Type

occurs
deficiency.

protein
com-

to be the limiting grains amino (30), there acids, (43). 60% in this musculature to changes,

acid

a common

acid

predominantly

on cereal of free responds ingested albumin) with

it is of interest is a sizeable particularly both acute of and

ponent giving concentration textured sponse These soy (34).

the highest value is the one containing of the deficient amino acid. Combinations proteins and beef protein have follow been this type

a higher of some of refrom rat

in the intracellular of this in the amount 50 g bovine for lysine 3 h. Hence,

Based of the low

on the data

nutritional

relationships

determined

of Bergstrom
(providing requirement within

et al (44), we calculate

that after a protein-rich


adult intracellular lysine

meal
daily pool content and the

bioassay studies. However, the more from human studies with soy and other plicability
knowledge

limited legumes in human foods


evaluate

results available confirm the apnutrition.


how nutritionally

be deposited

of
helps

this

general

concept
and

This

a protein

a relatively

us to understand

(maize)
tary, is to of the
Overall,

could
higher amino
the

be ingested
lysine-containing in the muscle mixture

some

hours
protein

later than
(eg, soy

a complemenprotein) content of maize.


would be

effective Our introduce proteins. about

combinations reason for

of plant discussing

protein amino acid

can

be achieved.

complementation

free-lysine

pool

would derived
of the

buffer from

the low lysine the digestion


meals

the question of timing There is some concern, the need to ingest different

of ingestion of complementary at least at the consumer level, plant proteins at the same time,

acid
nutritional

quality

combined

high.

or within the same tional value from amino acid patterns.

meal, to achieve maximum benefit and nutriproteins with different, but complementary, This concern may also extend to the question

We conclude profile at each of total protein

that it is not necessary to balance the amino acid meal, especially under conditions where intakes substantially exceed minimum physiological re-

1210S TABLE Plant

YOUNG II proteins in human nutrition: myths Myth and realities

AND

PELLET!

Reality (ie lack specific proteins amino acids) 1 ) Usual food dietary proteins combinations may be low of proteins in specific are amino complete: acids specific

I ) Plant 2)
3)
Plant

proteins proteins

are

incomplete

are not as

good

as animal

2 ) Quality depends on the source and dietary proteins: can be equivalent to high-quality in
3 ) Proteins do not need to be consumed at the

mixture animal
same

of plant proteins
time, the

Proteins from different plant foods must be consumed together the same meal to achieve high nutritional value 4 ) Animal bioassay procedures are satisfactory indexes of the human nutritional value of food proteins 5) Plant proteins are not well digested 6 ) Plant proteins alone (protein intake) 7) Plant proteins value are

4)

balance Animal

over a day is of greater importance bioassay procedures can be useful


plant can can vary protein nutritional according to source

but they may


for food humans preparation: and

underestimate

quality

5 ) Digestibility
digestibility

be high

are not sufficient

to achieve

an adequate

diet

imbalanced

and this limits

their nutritional

6 ) The intakes and balance of intakes of indispensable amino acids and nitrogen are crucial and can be adequately met from plant or plant and animal sources 7) There is no evidence that amino acid imbalances per se are
important: amino acid possible imbalances but can this be created is not by inappropriate a practical problem supplementation,

Downloaded from ajcn.nutrition.org by guest on March 24, 2014

quirements. Consumption of complementary proteins at different meals over the course of the day should assure the achievement of an adequate state of nitrogen (protein) retention and utilization. Therefore, an undue meal is inappropriate ulations. Protein digestibility and amino acid asailabilirs source may not be of its amino acid the utilization of emphasis on amino acid balance at each in the context of usual diets in healthy pop-

individual amino acids of plant foods. on the chemical and physical changes

More basic work is needed that occur in proteins under

these conditions and their nutritional effects to develop. in the long-term, optimum procedures for the utilization of plant food proteins. Many favorable cluding
foods eliminating essing,

plants

contain

numerous

compounds

that

may

cause

un-

physiological and clinical responses when eaten. indiminished digestibility. Man has learned to avoid those that produce
the or cooking,

The nutritional value predicted with precision content alone; several

of a dietary protein from a determination other factors can affect

immediate
undesirable results in the

ill effects
compounds destruction,

or has devised
from others. inactivation,

means
Often proc-

of

or less-

proteins. An important factor, feeding of simple-stomached and availability of the protein In general, the digestibility

which is frequently critical in the farm livestock, is the digestibility and individual amino acids. of vegetable proteins in their nat-

ening

of these

toxic

compounds reduced if novel

(antinutritional to eliminate plant foods

factors),

but they

may not be sufficiently entirely, particularly quently and over the factors present
their possible

the health problem are eaten more freExamples protein


significance

ural form is lower than that of animal proteins. Table 10 summarizes results for the digestibility in human subjects of various plant sources and of diets based on mixed plant-food sources. Plant proteins are often consumed only after undergoing some degree essing here, plant of preparation or processing. Although the effects of procon protein quality and availability will not be reviewed this foods factor for deserves humans. attention For example, in an overall oil-seed assessment flours recover favor and wheat foods. short-time heating, However, may on the may of be

longer periods of time. in various legume-seed


and physiologic

of some of sources and


are: amy-

metabolic

lase fere

inhibitors, which are found in most legumes and may interwith starch digestion; cyanogen. which is found in lima tannins, which and may form that are comany nutritional or

beans and may cause respiratory failure: and arc phenolic compounds found in most legumes less digestible complexes (45). In products mercially available these factors do not they and pose clinical problems. Nevertheless, in the course of developing new protein, sorghum for example, (46).

products from the cient tended their marily processing essing and of such enhanced spray for

of processes seed. Such human

designed processes feeding are

to economically do not necessarily protein. cooked Cereals or processed

the oil the effiinpri-

are important to consider improved sources of plant of new varieties and uses of

recovery palatability in bread,

of high-quality and pasta, that such have acceptance. and use

legumes to enhance is used Thermal

as in the case

For example, high-temperature, microwave adopted. that

breakfast-cereal-type

Summary
In this proteins brief the within protein protein

and
brief

conclusions
review we have highlighted nutrition. made a worldwide the We by plant basis value began and of plant with also a to proteins

methods conditions, drying, treatments, or reduced

procpuffing, as a result be either protein duBoilin relation consideration component to human protein on

as extrusion, been widely value

the nutritive

of the protein depends

of the contribution of diets

to an extent

components in the food and factors ration of heating, and the presence ing in water generally or dry heating reduces improves protein

such as the temperature, or absence of moisture. quality, Hence, the on the

the United States. We and for indispensable

then discussed amino acids

the requirements for in humans at various

protein quality. concerning conditions

whereas toasting it is difficult to effects of various proteins and the

draw broad generalizations processing and preparation

ages, together with a short survey of the amino acid composition of different plant-food protein sources. There is a large variation in the contribution made by plant proteins to the availability and intake of total dietary protein among populations both within the

PLANT technically developing amino plant diets well cereals, total lysine a major of such plant of amino quirements. acid proteins worldwide be limiting, for dietary protein and diets energy foods advanced regions. composition are a major regions It can of the world be shown of the major determinant from food and between protein lysine these sources content might where of the can have and of the that of

PROTEINS

12115

considerations

of the

(29, 30). This indispensable amino acid or marginal, in diets of some countries wheat, supply. such are the predominant modest or animal amounts proteins, source However, as legumes

example,

of higher-

10. Food and Nutrition Board, National Research Council. Assessment of protein nutriture. Washington, DC: National Academy Press, 1974. I 1. Food and Agriculture Organization/World Health Organization! United Nations University. Energy and protein requirements. Report of joint FAO/WHO/UNU expert consultation. Geneva: World Health Organization. 1985. (WHO Tech rep ser no 724.) 12. Food and Agriculture Organization. Amino acid content of foods and biological data on proteins. Rome: Food and Agriculture Organization. 1985. (FAO nutritional studies no 24.)

favorable impact on the protein (30). Overall it can be concluded can serve that as a complete meet and effectively human

nutritional quality that mixtures of source rephysiological

proteins acids

well-balanced

We present
plant sider issue and proteins a reference

in Table
in human to amino

11 a list of myths
nutrition. imbalance largely problem data We (no. acid

and realities
have included 7) that

concerning
in this list

we did not con-

in any detail earlier, to be an important interesting experimental

because we do not consider this in practice (47). Considerable have defined the nature and imbalances (48) of an imbalance and the unhave been high trials of leucine might be

13. US Department of Agriculture. Agricultural handbook no. 8-1 (1976); 8-2 (1977); 8-5 (1979); 8-6 (1980), 8-8 (1982); 8-9 (1982); 8-10 (1983); 8-1 1 (1984); 8-12 (1986) and 8-14 (1986). Washington, DC: Agriculture Research Service. 14. Pellett PL, Shadarevian S. Food composition tables for use in the Middle East. 2nd ed. Beirut: American University of Beirut, 1970. 15. Pellett PL, Young yR. Nutritional evaluation of protein foods. Tokyo: The United National University. 1980 (Publication No WHTR-3IUNUP-129.) 16. Osborne TB, Mendel LP, Ferry EL. A method of expressing numerically the growth promoting value of proteins. J Biol Chem 1919;37:223-9.

Downloaded from ajcn.nutrition.org by guest on March 24, 2014

mechanisms of dietary amino acid toward physiological consequences observed dietary intakes, in children protein (49). as supplied

17.

Young

yR.

Protein

nutritional

value

of soy proteins

in adult

humans.

during amino acid supplementation However, the suggestion that by sorghum in regions

In: Steinke FH, Waggle DH, Volgarev in human health: nutrition, prevention
CRC Press, 1991;107-19.

MN, eds. New protein foods and therapy. Boca Raton, FL:

of India,

etiologically significant in the pellagra that exists in these areas (50) has not been substantiated by considerable additional investigation amino for (47). acid meeting Thus, supply we about is from conclude amino the that acid plant-food consumers imbalances proteins the do not when that need make to up be at all concerned the dietary

18. Young yR. Soy protein in relation to human protein and amino acid nutrition. J Am Diet Assoc 1991;91:828-35. 19. Food and Agriculture Organization/World Health Organization. Protein quality evaluation. Report of a joint FAO/WHO expert consultation. Rome: Food and Agriculture Organization, 1991. (FAO food and nutrition paper No 51.) 20. Block Ri, Mitchell HH. The correlation of the amino-acid composition 21. of proteins with their nutritive value. Nutr Abstr Rev

our usual
composition

diets.

Mixtures

of plant
diet,

proteins
From they serve

can be fully
standpoint as a desirable

adequate
of the vehicle
El

human

requirements.

of a healthful

for carrying
our needs

nitrogen
and wants

and indispensable
(Table 11, reality

amino
no. 6).

acids

to meet both
22.

1946; 16:249-78. Food and Agriculture Food and Agriculture No 16.)


Food and Agriculture

Organization. Organization,
Organization/World

Protein requirements. 1957. (FAO Nutrition


Health Organization.

Rome: Studies
En-

References
23.

ergy and protein requirements. Report of a joint FAOIWHO ad hoc expert committee. Geneva: World Health Organization, 1973. (WHO Tech Rep 5cr no 522.) Young yR. Bier DM, Pellett PL. A theoretical basis for increasing
current estimates VR, of the amino JS. acid requirements and in adult nutritional man, significance with

H. Seeds of change. New York: Harper and Row, 1987. 2. Voelker TA, Worrell AC, Anderson L, et al. Fatty acid biosynthesis redirected to medium chains in transgenic oilseed plants. Science
1991;257:72-4.

1. Hobhouse

experimental
24. Young

support.
Marchini

Am J Clin Nutr
Mechanisms

1989;50:80-92. and amino acids, Am J Clin Nutr

3. Jones JL. Genetic engineering of crops: its relevance to the food industry. Trends Food Sci Technol 1992;3:54-9. 4. Benner MS. Phillips RL, Kirihara JA, Messing JW. Genetic analyses of methionine-rich storage protein accumulation in maize. Theor Appl Genet 1989:78:761-7. 5. Food and Nutrition Board, National Research Council. Diet and health: implications of reducing chronic disease risk. Washington, DC: National Academy Press, 1989. 6. Food and Agriculture Organization/Agrostat. Computerized information series No 1. Food balance sheets. Rome: Food and Agriculture Organization, 1991.
7. Consumer Nutrition Division, Human Nutrition Information Ser-

of metabolic responses to altered intakes of protein with reference to nutritional adaptation in humans.
1990;51:270-89.

25.

Marchini JS, Cortiella J, Hiramatsu T, Chapman TE, Young yR. Requirements for indispensable amino acids in adult humans: longer-term amino acid kinetic study with support for the adequacy of the Massachusetts Institute of Technology amino acid requirement pattern. Am J Clin Nutr 1993;58:670-83.
Zello GA, Pencharz PB, Ball RO. Phenylalanine flux, oxidation,

26.

and conversion 3Cjphenylalanine.


27. Zello GA, Ball RD,

to tyrosine in humans studied Am J Physiol 1990;259:E835-43.


Pencharz PB. Dietary lysine

with

L-[ 1deter-

requirement

vice. Food Hyattsville, no 1-1.)


8.

intakes in individuals MD: US Department

in 48 states. Year 1977-1978. of Agriculture, 1983. (Report

28.

Young VR, Pellett PL. Protein intake and requirements with reference to diet and health. Am J Clin Nutr 1987;45:1323-43. 9. Young VR. Protein and amino acid requirements in humans: metabolic basis and current recommendations. Scand J Nutr 1992;36:4756.

mined by phenylalanine flux and oxidation. Proc Nutr Soc Aust 1991; l6:32(abstr). Young yR. Pellett PL. Protein evaluation, amino acid scoring and the food and drug administrations proposed food labeling regulations. J Nutr 1991;121:145-50.
Bressani ET, R. Nutritive value of high lysine cereals In: Ejita G, Mertz

29.

Rooney International
Lafayette, IN:

L, Schaffert Conference
Purdue

R, Yohe J, eds. Proceedings on Sorghum Nutritional Quality.


1992:50-74.

of the West

University,

12125 30.

YOUNG

AND

PELLET! 41. Young VR. Nutrient protein metabolism tein-energy relations


Taylor YSM, Young

Young yR. Pellett PL. Current concepts concerning indispensable amino acid needs in adults and their implications for international planning. Food Nutr Bull 1990;12:289-300. 31. Torun B. Soy proteins as amino acid and protein sources for preschool-age children. In: Steinke FH, Waggle DH, Volgarev MN, eds. New protein foods in human health: nutrition, prevention and therapy. Boca Raton, FL: CRC Press, 1992;91-100.
32. Fomon SJ, Ziegler EE. Isolated soy protein in infant feeding. In:

interactions with reference in non-ruminants: particular in man. Zeit Ernahrungswiss


VR, Murray E, Pencharz

to amino acid and emphasis on pro1991;30:239-67.


PB, Scrimshaw NS.

42.

FH, Waggle DH, Volgarcv MN, eds. New protein foods in health, nutrition, prevention and therapy. Boca Raton, FL: CRC Press, 1992;75-83. 33. Bressani R, Elias LG, Gomez Brenes RA. Improvement of protein quality by amino acid and protein supplementation. In: Bigwood El, ed. Protein and amino acid functions. Vol 11. Oxford, UK: Pergamon Press, 1972;475-540. 34. Kics CV, Fox HM. Effect of varying ratio of beef and textured vegetable protein nitrogen on protein nutrition value for humans. J Food Sci 1973;38:1211-3.
35. Geiger E. Experiments with delayed supplementation of incomplete

Steinke human

Daily protein and meal patterns affecting young men fed adequate and restricted energy intakes. Am J Clin Nutr 1973;26: 1216-21. 43. Munro FIN. Free amino acid pools and their role in regulation. In: Munro HN, ed. Mammalian protein metabolism. Vol 4. New York: Academic Press, 1970:299-386. 44. Bergstrom J, Furst P, Vinnars E. Effect of a test meal, without and with protein, on muscle and plasma free amino acids. Clin Sci
1990;79:331-7.

45.

46.

amino acid mixtures. J Nutr 1947;34:97-111. 36. Geiger E. The role of the time factor in feeding teins. J Nutr 1948;36:813-9.
37. Yang SP, Steinhauer JE, Masterson JE. Utilization

Liener IE. Antinutritional factors in legume seeds: state of the art. In: Huisman J, van der Pod TFB, Liener IE, eds. Recent advances of research in antinutritional factors in legume seeds. Wageningen, The Netherlands: Pudoc 1989:6-13. Kirleis AW. The prolamins of sorghum: their role in protein digestibility. In: Ejeta G, Mcii ET, Rooney L, Schaffert R, Yohe J, eds. Proceedings of the International Conference on Sorghum Nutritional Quality. West Lafayette, IN: Purdue University, 1990:168-76.
Young VR, Fukagawa NK. Amino acid interactions: a selective re-

supplementary
of a delayed

proly-

47.

sine supplement 38. Yang SP, Tilton


tryptophan 1968;94:178-84.

by young rats. J Nutr 1963;79:257-61. KS, Ryland LL. Utilization of a delayed


for protein repletion of rats.

48. lysine
J

view. In: Bodwell CE, Erdman JW Jr, eds. Nutrient interactions. New York: Marcel Dekker, Inc, 1988:27-71. Harper AE, Benevenga NJ, Wolheuter RM. Effects of ingestion of
disproportionate amounts ofamino acids. Physiol Rev 1970;50:428-

Downloaded from ajcn.nutrition.org by guest on March 24, 2014

or
Nutr

supplement

49.

39.
40.

Batterham ES. The effect of frequency of feeding on the utilization of free lysine by growing pigs. Br J Nutr 1974;31:237-42. Batterham ES, ONeill GH. The effect of frequency of feeding on the response by growing pigs to supplements of free lysine. Br J Nutr 1978;39:265-70.

50.

558. Scrimshaw NS, Bressani R, Behar M, Viteri F. Supplementation of cereal protein with amino acids. Effect of amino acid supplementation of corn-masa at high levels of protein intake on the nitrogen retention of young children. J Nutr 1958;66:485-99. Gopalan C, Srikantia SG. Lcucine and pellagra. Lancet 1960;1:9S47.

Anda mungkin juga menyukai