Some confusion exists over the use of certain terms connected with the energy value of foods, such as “available” and “metabolizable” energy. Excellent accounts of the historical background to, and the current use of, these terms are given by Merrill & Watt (1) and are summarized by Widdowson (2). These accounts refer to the derivation and use of the classical Atwater factors for the energy values of carbohydrate, protein, and fat. The application of these values varies slightly in tables of food composition complied in the United States of America (and other countries using a similar system) and those used in the United Kingdom. These differences will be discussed briefly below.
The amount of energy contained in the energy-yielding nutrients of foods (carbohydrate, fat, and protein) and in alcohol can be expressed in two ways:
(a) The gross energy is the energy released as heat when the particular food is completely combusted in a bomb calorimeter. This value can also be calculated if the chemical composition of the food is known, by applying the gross energy value of carbohydrate (4.1 kcalth or 17 kJ per g), fat (9.3 kcalth or 39 kJ per g), and protein (5.4 kcalth or 23 kJ per g) to the amounts of these nutrients in the food. These values are only approximations, since they will vary slightly depending on the particular carbohydrates, fats, and proteins present.
The energy values given above are not those available to the body, since some of the ingested energy is lost. For protein, about 1.25 kcalth (5.2 kJ) is lost as nitrogenous substances in the urine. Therefore the “gross” energy for protein is usually taken as 4.1 kcalth (17 kJ) per g. Further losses occur, since small amounts of the nutrients are either undigested or not absorbed and are excreted in the faeces.
Measurement of the gross energy content by bomb calorimetry is mainly used in balance studies, where intakes and losses in the urine and faeces are measured simultaneously. It should be also noted that when estimates of the energy cost of growth are being made, it is the values for gross energy that should be used to calculate the energy content of the tissue laid down, according to the first law of thermodynamics: F = H + W + S + L (where F = energy from food, H = heat production, W = external work, L = losses, and S = energy stored).
The metabolic “available” energy discussed here is not to be confused with the term available energy sometimes used in the thermodynamic literature, meaning the free energy (Gibbs energy).
(b) The term available energy refers to the amount of energy present in food as carbohydrate, fat, and protein, minus the amount present in the faeces. For protein, the 1.25 kcalth (5.2 kJ) per g lost in the urine is also deducted. The Atwater factors for available energy—4.0 kcalth (17 kJ) per g for protein, 4.0 kcalth (17 kJ) for carbohydrate, and 9.0 kcalth (38 kJ) for fat—were determined from the average values for these losses on habitual American diets.
The available energy of a food, determined as intake minus losses, is not the same as its true digestibility. This difference arises because when faeces are analysed for undigested food residues the latter cannot be distinguished from similar endogenously derived substances such as desquamated cells and various nitrogenous compounds, fatty acids, etc., some of which are contained in the bacteria, for example. The true digestibility can be approximated by measuring the faecal energy loss in the absence of food (endogenous loss) and subtracting this value from the faecal loss in the presence of food.
It is the available energy which is of practical interest when considering whether food will meet the requirements. It should be clearly understood that the available energy, as defined above, depends on both the characteristics of the food and the body's reaction to it. Thus any condition of the body or any property of food that either impairs digestion and absorption, or increases the endogenous losses, will reduce the availability of energy. In this report we are not concerned with pathological conditions that result in malabsorption. Nevertheless, even in normal subjects the same diet may provide different amounts of available energy to different people. There is evidence, for example, that a diet high in fibre may be utilized more efficiently by those who are habituated to it (3) (see section 7.1.3). Conversely, in populations in tropical countries, persistent low-level infection and parasitization of the gut may reduce the availability to the body of the energy provided in the food.
7.1.2 Expression of available energy
Most tables of food composition give only the available energy. The interpretation of these values may vary, depending on the basis of calculation, which should therefore always be specified. Particular problems arise in relation to carbohydrate. Many tables of food composition calculate the quantity of carbohydrate in food “by difference”. That is, the carbohydrates are not chemically analysed but the quantity is obtained by assuming that the food, once the water content has been measured, is made up of fat, protein, and ash and that the remainder is carbohydrate. Water content is measured, together with the fat, protein, and ash content and the difference between this total weight and the initial weight of the food is assumed to be carbohydrate with an overall energy value that is usually 4.0 kcalth (17 kJ) per g. Some tables, e.g., those in common use in the USA, employ the Atwater specific factors for different types of carbohydrate.
Tables of food composition in the United Kingdom are formulated, to a varying but increasingly more comprehensive extent, on the actual chemical analyses of the different carbohydrates —sugars, starch, pentosans, celluloses, lignin, etc. (4). Some of these carbohydrates are superficially “unavailable” to the human body because no enzymes are present in the digestive juices to digest fibre. The United Kingdom tables therefore, being based on the direct measurement of the “available” carbohydrates, express these as monosaccharides with an energy value of 3.75 kcalth (16 kJ) per g.
The energy value of the same foods will therefore differ slightly between the various tables of food composition.
7.1.3 The effect of dietary fibre on available energy
These differences may be important in groups of people whose diet contains large amounts of fibre or “unavailable” carbohydrate, particularly if the total energy content of the diet is low. The quantitative effect of fibre on the availability of dietary energy is at present unclear. Considerable amounts of fibre may be broken down by the action of bacteria in the gut, producing fatty acids and heat, both of which may contribute to the energy economy and thus to energy requirements.
This effect may be important in two completely different circumstances: in many developing countries, where the diet contains much fibre from vegetables, whole-grain meal, root crops, and fruits; and in developed countries, where the recent emphasis on the nutritional importance of fibre in the diet has resulted in large numbers of persons eating diets containing whole-wheat bread, fruits, and vegetables in considerable quantities. In both cases, there are problems in determining the available energy of the diet from the tables of food composition in use at the present time.
There is also a certain amount of evidence that fibre in the diet may reduce the apparent available energy from fats and proteins. When moderate amounts of fibre are introduced into the diet as wholemeal bread, fruit, and vegetables, small reductions in the energy value of all the nutrients occur, amounting to an overall fall of 2–3% in the availability of dietary energy. Further increases in the fibre content of the diet, with fruit and vegetables at the levels consumed by vegetarians, result in an additional 2–3% reduction in available energy (5).
From these findings it is suggested that no extra correction need be made to the energy available from food if the value is calculated from any food composition tables based on the Atwater factors, and if the diet contains only small amounts of fibre. When diets contain moderately large amounts of fibre, derived from fruit, vegetables, and wholemeal bread, values for available energy calculated as above should probably be reduced by about 5%. This adjustment may not be enough for diets containing the high levels of fibre typical of some populations in developing regions of the world.
Energy density is defined as the energy content per gram of food. The energy density of traditional foods in many developing countries is a critical factor in the translation of estimates of dietary needs into practical food intakes. This is largely because of their low fat and, frequently, high water content (4). In surveys of food intake, which depend upon food tables for interpretation, the water content of cooked foods should be measured whenever possible, as this component represents a major potential source of error and inaccuracy. A simple field procedure for this purpose has been described (6).
Another characteristic of food that is important in relation to the fulfilment of requirements is its consistency, or the ease with which it can be eaten, particularly by the young child. This property is related to energy density, since cereal porridges, particularly when prepared from maize, tend to be very glutinous unless made into a thin gruel by adding water. This naturally reduces the energy density. However, the addition of a small amount of vegetable oil to these porridges has a remarkable effect in making them less glutinous, while at the same time increasing the energy density (7).
If substances such as fat and sugar are added to increase the energy density and palatability of food, care must be taken to ensure that the concentrations of protein and other nutrients are not reduced to unacceptably low levels (see section 10).
The intake of 0.75 g of protein/kg body weight estimated as the safe level for adults, with corresponding intakes for other age groups, refers to proteins with amino acid compositions providing adequate amounts of essential amino acids and having a high degree of digestibility. These conditions are satisfied by the proteins of hen's egg, cow's milk, meat, and fish. To apply the recommended safe intakes of protein to diets containing other protein sources consumed by populations throughout the world, it is necessary to consider the essential amino acid patterns provided by their mixed dietary proteins, and their availability in terms of digestibility. Upward adjustments in the recommended intakes may then be made where necessary to allow for these factors.
7.3.1 The protein content of foods
In this report the determination of protein requirements is based on nitrogen balance, involving the measurement of total nitrogen in the food and excreta. Strictly speaking, therefore, the requirement as determined is for nitrogen rather than for protein. The convention used in food composition tables is to measure total nitrogen in a food, usually by a Kjeldahl-type procedure, and to multiply this by a factor to calculate the protein content of the food. Since most proteins contain about 16% nitrogen, total dietary nitrogen multiplied by 6.25 will give a reasonable estimate of protein intake. In strict terms, this should be referred to as “crude protein”.
Some proteins contain a higher or lower percentage of nitrogen and some foods also contain non-protein nitrogen. The nitrogen content of a range of isolated proteins has been measured and conversion factors derived for many food proteins (8, Annex 3).
These specific nitrogen conversion factors may be applied to allow the precise comparison of the amino acid composition of foods, but for purposes of relating intake to requirement, N × 6.25 is the appropriate factor, since this is the factor from which requirements were determined.
To determine protein digestibility, measurements of the nitrogen in food and faeces are made. “Apparent protein (N) digestibility” or “true protein (N) digestibility” are calculated as follows:
|where||I = nitrogen intake|
|F = faecal nitrogen output on the test diet|
|Fk = faecal nitrogen output on a non-protein diet.|
The value of Fk need not necessarily be determined directly if the diet contains only a small amount of fibre. The Consultation accepted a value of 12 mg of N/kg per day as an estimate of Fk in adult men and women receiving diets without excessive amounts of fibre.
Differences in digestibility may arise from intrinsic differences in the nature of food protein (nature of cell wall), from the presence of other dietary factors which modify digestion (dietary fibre and polyphenols, including tannin), and from chemical reactions that alter the release of amino acids from proteins by enzymatic processes. Differences in digestibility affect the utilization of protein, so that an adjustment for digestibility is necessary when translating requirements for reference proteins to safe levels of intake of ordinary mixtures of dietary proteins. Table 36 provides representative data on the true digestibility of proteins; more extensive data are given elsewhere (9). Since estimates of safe levels of intake are based on data derived from feeding milk, egg, meat, and fish proteins, it is appropriate to express the digestibility of other proteins in relation to that of egg, milk, etc., as shown in Table 36.
Large intakes of dietary fibre, especially hemicelluloses and cereal brans, increase the excretion of nitrogen in the faeces, reducing the apparent protein digestibility by about 10% (4). Thus the overall composition of the diet must be taken into account when assessing digestibility.
|Protein source||True digestibility|
(mean ± SD)
|Milk, cheese||95±3 95||100|
|Maize + beans||78||82||b|
|Maize + beans + milk||84||88||b|
|Indian rice diet||77||81||(10)|
|Indian rice diet + milk||87||92||(10)|
|Chinese mixed diet||96||98c||(11)|
|Brazilian mixed diet||78||82||(12)|
|Filipino mixed diet||88d||93||(13)|
|American mixed diet||96d||101||(14)|
|Indian rice + beans diet||78d||82||(15)|
a Except as indicated all figures are from reference (9).
b Viteri, F., unpublished data, 1971.
c Relative to egg measured in the same study.
d Recalculated from apparent digestibility, using Fk = 12 mg N/kg (see text).
If information is not available on the digestibility of the protein in a particular diet, the value can be estimated by using values for individual foods and calculating a weighted mean according to the proportion of protein supplied by these foods. Table 37 provides an example of this approach. Alternatively, for diets based on coarse, whole-grain cereals and vegetables, a correction for digestibility of 85% may be applied, and for those based upon refined cereals the correction is 95%.
These corrections can be applied either to the requirement or the diet. In the report of the 1971 Committee (8) the former was recommended, so that the safe level of dietary protein was taken as: safe level of reference protein × 100% digestibility with reference to milk, egg, or meat. However, for comparing intakes with safe levels it is often more convenient to correct the intake. Thus: digestible protein = actual dietary protein (N × 6.25) × % digestibility/100.
|Food||Fraction of |
to reference proteins
Digestibility of total protein in the diet =
(0.4 × 93) + (0.1 × 89) + (0.35 × 82) + (0.1 × 100) + (0.05 × 100)
7.3.3 Amino acid scoring pattern
The requirements for essential amino acids at various ages have been discussed in section 5.6. The concentrations of essential amino acids in food proteins are considered in this section in relation to the extent to which they meet the needs of subjects at different ages.
The Consultation, like its predecessors, accepted the evidence of a relationship between the amino acid composition of proteins and their nutritional value. Thus, if the composition of an “ideal” protein, i.e., one containing all the essential amino acids in amounts sufficient to meet requirements without any excess, were known, it should then be possible to compute the nutritional quality of a protein or mixture of proteins by calculating the deficit of each essential amino acid below the amount in the “ideal” protein. This approach is the basis of the so-called amino acid scoring procedure, by which one can evaluate the capacity of a given protein or mixture of proteins to meet the essential amino acid and nitrogen requirements of the recipient. It must therefore be based on knowledge of those needs.
Current estimates of amino acid requirements (in mg/kg per day) at different ages are shown in Table 4, and in Table 38 the patterns of amino acid requirements in mg/g of protein are compared with the concentrations in milk, egg, and beef. These patterns are different from those tabulated in the report of the 1971 Committee (8), even though the estimates of amino acid requirements (in mg/kg body weight) are essentially unchanged. This is because the safe levels of protein intake adopted by the present Consultation are different from the earlier values. The total protein levels now accepted for adults and schoolchildren are higher than the figures of the 1971 Committee and therefore the essential amino acids required per gram of protein are correspondingly reduced.
(mg/g crude protein)
|Suggested pattern of requirement||Reported compositionc|
|Methionine + cystine||42(29–60)||25||22||17||57||33||40|
|Phenylalanine + tyrosine||72(68–118)||63||22||19||93||102||80|
a Amino acid composition of human milk (16–19).
b Amino acid requirement/kg divided by safe level of reference protein/kg (Tables 4, 33, and 34).For adults, safe level taken as 0.75 g/kg; children (10–12 years), 0.99 g/kg; children (2–5 years), 1.10 g/kg. (This age range is chosen because it coincides with the age range of the subjects from whom the amino acid data were derived. The pattern of amino acid requirements of children between 1 and 2 years may be taken as intermediate between that of infants and preschool children).
c Composition of cow's milk and beef (16) or egg (Lunven, P. et al., unpublished data, 1972).
d Values in parentheses interpolated from smoothed curves of requirement versus age.
|Indian diets, vegetarian (research)|
|Tunisian diets, wheat-based (survey)|
|Brazilian diets, south (survey)|
|Guatemalan diets (research)|
|Maize 76%/beans 24%||38||31||37||7||(23)|
|Mexican Tarahumara Indian diet (survey)|
|Nigerian diets (research)|
|Cassava-based No. 1||42||24||30||11||(22)|
|Cassava-based No. 2||63||34||37||12||(22)|
a Perissé, J. et al., unpublished data, 1981.
b François, P., personal communication, 1982.
For infants, the Consultation concluded that the amino acid pattern of human milk should be accepted as the requirement. It is evident that the amino acid content of the high-quality proteins more than meets the suggested requirement patterns of all other age groups.
Proteins and diets with an essential amino acid content and pattern that effectively meet the needs of infants and young children will also be adequate for older children and adults, whereas the converse may not be true. Only four essential amino acids are likely to limit the protein quality of mixed human diets: lysine, the sulfur-containing amino acids (methionine+cystine), threonine, and tryptophan. In Table 39 human requirements are compared with concentrations of these amino acids in diets representing those eaten in the developing countries. None of the diets listed fails to meet the amino acid requirements of adults. Thus, it is necessary to adjust protein allowances to take account of the amino acid requirements of children, but not of adults. For adolescents the position is not clear since information is not available on amino acid requirements during the phase of rapid pubertal growth. This is a subject for future research.
To adjust the safe level of protein to take into account the amino acid composition, a score must be calculated according to the most limiting amino acid, i.e., the one in greatest deficit for the age group involved. The amino acid score is calculated as a “percentage of adequacy”, as follows:
Amino acid scores calculated from the representative diets listed in Table 39 are given in Table 40.
In the report of the 1971 Committee (8) the amino acid score was calculated without taking account of digestibility and as a result the score will somewhat overestimate the capacity of protein to meet physiological requirements. In accordance with the suggestion of the 1975 informal gathering of experts (23), and in view of the importance, discussed earlier, of the digestibility of proteins in mixed diets, calculation of the capacity of a diet to meet the protein requirement now incorporates both an estimate of the digestibility of the protein and the amino acid score.
As with digestibility, the correction for the amino acid score can be applied to either the requirement or the diet. An example of adjustment by both methods for three age groups is shown in Table 41.
|Diet||Preschool child||School-age child|
|Lysine||Meth.+ cys.||Threonine||Tryptophan||Lysine||Meth.+ cys.||Threonine||Tryptophan|
|Indian diets (vegetarian)|
|Maize 76%/beans 24%||66||*||*||64||86||*||*||*|
|Mexican Tarahumara diet|
* Composition supplies 100% or more of the requirement.Limiting amino acid in italics.
For infants younger than 1 year the scoring pattern should be based on the amino acid composition of breast milk. The pattern of amino acids in breast milk is richer in total sulfur-containing amino acids than cow's milk. However, infants consuming cow's milk proteins at the same level (24, 25) as breast milk show satisfactory growth and nitrogen balance. Consequently, for dietary proteins limited in sulfur-containing amino acids, the use of a scoring pattern based on breast milk may slightly underestimate their capacity to meet the physiological requirements of the infant.
|Amino acid score: preschool child (2–5 years)||=||57|
|schoolchild (10–12 years)||=||75|
|Digestibility: unknown, assume 85|
|A. Calculation of safe level of dietary protein as consumed.|
|Safe level of reference protein||=||1.10 g/kg|
|Safe level of dietary protein||=|
|Safe level of reference protein||=||0.99 g/kg|
|Safe level of dietary protein||=|
|Safe level of reference protein||=||0.75 g/kg|
|Safe level of dietary protein||=|
|B. Calculation of effective amount of protein consumed in terms of reference proteins (milk, egg).|
|Corrected protein intake||=|
|=||intake × 0.48|
|Corrected protein intake||=|
|=||intake × 0.64|
|Corrected protein intake||=|
|=||intake × 0.85|
The pattern for preschool children should be used for ages 1–6 years, and the schoolchild pattern for ages 6–12 years. Over the age of 12 there is no evidence that a correction for amino acid composition is required with usual mixed diets. However, this is a subject on which more work is needed. The protein content of infant formulae may vary and, indeed, can be adjusted to compensate for a lower concentration of essential amino acid per unit of nitrogen, relative to that in breast milk. Thus, in using calculations of the amino acid score to assess the nutritional value of an infant formula account must be taken of the total amount of protein (and amino acids) provided by the formula, relative to the intake supplied by breast-milk protein.
The amino acid requirements of pregnant and lactating women have not been determined. Obviously, the essential amino acids deposited in fetal and maternal tissues and secreted in milk must be supplied in the diet.
One approach to the development of theoretical amino acid requirements for lactation has been examined by the Consultation. The safe level of protein for a 55-kg woman is 55 × 0.75, or 41 g/day; the addition for lactation is 16 g/day. Thus, the lactating woman needs 57 g of protein per day, of which 72% (41/57) represents her maintenance requirement, and 28% (16/57) the requirement for milk-protein secretion. By multiplying the factor 0.72 by the adult amino acid pattern and 0.28 by the breast-milk amino acid composition the following pattern per g of dietary protein is obtained for a representative lactating woman:
|Adult pattern||Milk pattern||Lactation pattern|
Information on the amino acid composition of tissues deposited during pregnancy would be needed to calculate a provisional pattern for pregnant women. However, this information does not exist, and therefore the amino acid requirements of this group is an important topic for further research.
7.3.4 Biological evaluation
The quality of a protein may also be evaluated by a biological test of N utilization. Many procedures have been tried and a discussion of the methods, together with their advantages and limitations, is given in the United Nations University publication, Nutritional Evaluation of Protein Foods (26). One of the most frequently used is the determination of net protein utilization (NPU); this is the proportion of ingested N that is retained in the body under specified conditions. NPU is a combined measure of digestibility and the efficiency of utilization of the absorbed amino acids. However, this test can be easily adapted to include a separate measure of digestibility.
The various methods may be criticized for a variety of reasons and the appropriate choice of a particular method will depend upon the intended purpose of the measurement. However, in reference to predicting the nutritional value of a protein source or mixture of sources for meeting human requirements, a number of limitations should be recognized. First, for example, some dietary proteins totally lacking in one or more essential amino acids still show a measurable NPU in rats. Secondly, it is both costly and time-consuming to determine the NPU of a food in experiments on man, and few centres are equipped to do so. Therefore most estimations are made on growing rats, whose amino acid requirements are different from and, in general, higher than those of man. This tends to underestimate the quality of some proteins for man, particularly adults.
With biological evaluation the safe level of intake of a particular food protein would be predicted from the formula:
In summary, digestibility appears to be the most important factor determining the capacity of the protein sources in a usual mixed diet to meet the protein needs of adults. Therefore in most cases a digestibility correction would be sufficient to predict safe protein intakes for adults. For young children corrections of the type described above (amino acid score or biological assay) would be appropriate, but a digestibility factor must always be included in making adjustments for safe protein intakes. However, these corrections should not be applied to the protein requirements of breast-fed infants since the nutritional value of proteins in human breast milk is accepted as being biologically ideal.
Energy expenditure will be increased if extra heat production is needed to maintain the body temperature in a cold climate. There is evidence from calorimetry studies (27) that when lightly-clad people are exposed to low ambient temperatures their basal metabolic rates are increased, even in the absence of shivering. Usually, however, such effects of cold are minimized by clothing.
Conversely, there is some evidence that the basal metabolic rate is reduced in hot climates. As mentioned above (section 4), the BMR is on average 10% lower in Indians than in North Europeans. There may also be a behavioural adaptation in the form of less energetic movements. In 1957 the second FAO Committee on Calorie Requirements (28) recommended that energy requirements should be decreased by 5% for each 10°C of mean annual external temperature above the reference temperature of 10°C, and that requirements should be increased by 3% for each 10°C below the reference temperature. That committee recognized, however, that the mean external temperature is a very inadequate measure of heat-load or the tendency to heat loss. In view of the scanty and conflicting information, the 1971 Committee did not recommend any adjustments to the energy requirement for differences in environmental temperature. The present Consultation accepts that view, although the subject is one that requires further study.
There is no information to suggest that requirements for protein are increased in the cold. On the other hand, in hot climates sweating causes an increased loss of nitrogen from the skin, since sweat contains an appreciable amount of N, mainly as urea. Very large losses of N by this route have been recorded in unacclimatized subjects exposed to heat under artificial conditions such as hot chambers (29). Such results cannot be extrapolated to people who live in tropical countries, since, with acclimatization to heat, sweat becomes more dilute, with lower concentrations of both sodium and nitrogen. Under these conditions losses in sweat have been estimated at 0.5–1 g of N per day (30, 31). There is some evidence that, as might be expected on physiological grounds, the increased clearance of N through the skin is compensated by decreased renal excretion. For this reason the Consultation does not consider that the protein requirement increases significantly in hot climates.
Although people who are suddenly exposed to high altitudes suffer anorexia, weight loss, and a reduction in aerobic capacity, these are temporary effects that disappear with acclimatization. There is no evidence that the requirements for protein or energy are altered in those who habitually live at high altitudes.