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close this bookProtein-Energy Requirements of Developing Countries: Evaluation of New Data (UNU, 1981, 268 p.)
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Protein requirements for adults

The working group on protein requirements for adults was asked to address the following major questions:

1. An important factor in the utilization of food proteins, especially of plant compared with animal sources, is their digestibility. What differences in faecal nitrogen exist between populations with low protein intakes corresponding to those used to measure obligatory losses at requirement levels, and populations with habitual levels of protein intake from different food sources?

2. What variation in nitrogen digestibility occurs with different diets and levels of dietary fibre in relation to various hygienic factors?

3 How should requirements, expressed as egg or milk protein, be adjusted for other protein sources and diets (i.e., of different nutritional quality)?

4 What is the significance of zero-balance intercepts for different diets and populations? What effect does inclusion of integumentary losses have on estimates of nitrogen balance and of protein requirements?

5. What are the effects of acute and chronic infections and of other stress situations?

6. What long-term indicators of dietary protein and energy adequacy are appropriate?

7. What reference protein source is appropriate for establishing requirements in adults?

The task force responded to these questions as follows.

1. Faecal Nitrogen

Mean values for endogenous faecal nitrogen loss reported by various groups range from 8 to 16 mg N/kg/day. It was thought that two factors might explain this variation.

First is the time at which measurements were made after initiation of the experimental, low-protein or protein-free diet, although the available data are not sufficiently extensive to assess the quantitative importance of this variable.

Second, the ingredient composition of the experimental diet may also influence the output of endogenous faecal nitrogen. Thus, in order to resolve the issue as to whether differences exist between specific population groups, a highly standardized diet would have to be used. However, a resolution of this problem would not be expected to contribute importantly to the further refinement of estimations of adult protein needs.

The limited data available do not suggest marked differences in faecal nitrogen between the groups of adults studied. There appears to be little need, therefore, to generate additional data on obligatory faecal nitrogen losses for the purpose of refining estimates of the protein requirement.

It has been customary to consider faecal nitrogen losses of individuals after brief adaptation to a nitrogen-free, but otherwise adequate, diet as representing obligatory losses; the latter are subtracted from faecal losses in calculating "true digestibility." There is no reason, however, for making such a correction when the object of the study is to determine the total amount of ingested nitrogen necessary to reach a defined level of body nitrogen balance. Moreover, there is no evidence to support the assumption that obligatory faecal losses measured on a nitrogen-free diet are representative of metabolic faecal nitrogen losses when the protein content of the diet approximates an intake in the requirement range. On the contrary, there are reasons to believe that this assumption is invalid.

Measuring the nitrogen balance at various levels of intake of usual diets avoids the problem. In other words, when attempts are made to determine the amount of dietary protein required for long-term nitrogen equilibrium, separate estimation of endogenous faecal nitrogen losses is unnecessary.

At requirement levels of intake with highly digestible protein sources and refined diets, faecal nitrogen output approximates 20 per cent of total nitrogen output and increases to about 35 per cent for diets containing predominantly vegetable protein sources. The available data from the current UNU sponsored studies, together with previous data from the Institute of Nutrition of Central America and Panama (INCAP) and other data from developed countries, suggest that there are minimal differences in mean faecal nitrogen losses between different groups of adults when highly digestible animal protein foods serve as the major source of protein intake. However, for diets based on vegetable protein sources, there appear to be larger differences in faecal nitrogen output both within and among the experimental populations comprising subjects from developed and developing regions. Among the possible dietary factors are kinds of protein (animal, mixed, or predominantly plant sources), levels of dietary fibre, presence of inhibitors of digestive enzyme activity, such as polyphenolic compounds, and the structural organization of the foods. In addition, the population differences observed may be due to the higher faecal nitrogen outputs arising from chronic, subclinical pathophysiological changes in gastrointestinal function and metabolism.

At habitual levels of protein and food intake that may provide protein at levels in excess of requirements, differences among populations may not be readily distinguishable, but there are no adequate data to evaluate this point.

2. Variation in Nitrogen Digestibility

As to variation in nitrogen digestibility with different types of diet, comparison among apparently healthy populations consuming the same diet indicates that differences in digestibility are due largely to differences in health, especially the reduced absorption due to what has been described as "tropical jejunitis" 11*). There is little evidence to indicate long-term and favourable adaptive responses of the gastrointestinal tract to poorly digestible diets by individuals or different ethnic groups. Furthermore, there is no good evidence that favourable adaptations in nitrogen digestion and absorption occur in response to conditions that initially result in poor nitrogen digestibility. Improvements over time can be achieved by appropriate health interventions or by upgrading the sanitary conditions of the environment.

3. Adjustment of Requirements for Various Protein Sources

The adjustment of requirements expressed as egg or milk protein for other protein sources and diets is necessary, according to data presented at this meeting. With diets based on mixed protein sources that include small amounts (10-25 per cent) of high quality protein, differences in protein requirements, relative to milk or egg as a reference, appear to be due mainly to differences in digestibility and absorption of ingested proteins. This observation underscores the importance of including digestibility, as proposed by the 1975 Consultative Group (2), in adjustments of protein quality based on a chemical score procedure.

The data presented at this meeting indicate that the mean requirement for a protein source of nutritional value equal to that of egg or milk protein is approximately 0.6 g/kg/day, or a value 30 per cent greater than that proposed in the 1973 FAD/WHO report (3).

An observation made in a number of these studies was that the efficiency of nitrogen utilization is low at very low protein intakes, in contrast to the experience reported in the literature (4) based on individual protein sources, such as egg or milk, and on studies in healthy Caucasian and Oriental subjects. This difference in the observations may reflect various factors: (a) an experimental design problem associated with rates of adaptation of nitrogen metabolism to different nitrogen intakes, and (b) biological and metabolic factors related to balance and utilization of amino acids. If this observation is biologically significant it will have important implications for protein nutritional status where people consume diets low in protein either on occasion or for more frequent or extended periods.

The problem of further exploring the rate of adjustment in nitrogen utilization to changes in source and level of nitrogen intake is not only a matter of significance in experimental design, but also possibly a problem that has importance in relation to the meal and daily pattern of protein intake to maintain an adequate protein nutritional status.

In reference to adults, an overview of the data at the meeting supports the appropriateness of correcting requirements for egg or milk to other protein sources of lower quality; this correction then applies to both adults and healthy, normally growing children. Protein quality adjustment factors must be developed and validated under test protein levels that approach maintenance requirements.

4. Zero-Balance Intercepts

For the measurement of zero nitrogen balance intercepts, three test levels are inadequate and four test levels represent a minimally acceptable design. In reference to zero nitrogen balance intercepts, estimates of balance should always include a specified level of integumentary loss, the level depending upon the particular environment under which the nitrogen balances were obtained. No data were presented at the meeting to substantiate the concept that there are quantitatively significant differences in protein requirements among genetically distinct groups of healthy individuals of comparable age and body composition.

5. Effects of Infections

Mild to moderate parasitic infestations of the gastrointestinal tract with helminths did not reveal unfavourable effects on nitrogen balance and utilization for generous protein intakes. The group felt that there is a continuing need to examine this issue in further studies involving levels of protein intakes that approximate requirements and to include other infestations, such as Giardia.

6. Long-term Indicators

The group agreed strongly that nitrogen-balance measurements do not provide a definitive evaluation of long-term protein requirements. There is an urgent need to examine the metabolic and health significance of nitrogen-balance data in critical detail.

In order to achieve this goal the most critical need is to define better the physiology of human protein and amino acid metabolism and its relationship to current measures of requirements, physiological function, and health status. This requires further basic research, specifically directed toward improving the definition of human protein and amino acid requirements and the factors that affect them.

This question must include exploration of the design of experimental protocols for assessing protein and amino acid requirements. The group considered that multiple approaches are necessary to arrive at a definite statement on these requirements, and that highly controlled metabolic studies involving both shorter- and longer-term diet periods play an important role in reaching this goal. However, the ultimate definition will require studies of populations living under natural environmental conditions, and these studies must incorporate improved measurements of food intake, as well as of the nutritional and health status of the members of the population.

Choice of Reference Protein

The question was raised by the drafting group as to whether there was evidence indicating a more adequate reference protein than milk or egg. This question was addressed, in part, because various investigators at the meeting have observed a relatively large variation in nitrogen-balance data when using egg, compared with other sources of protein tested. Although the group did not re-examine the data in specific detail, it was their tentative conclusion that there is no justification for recommending high quality protein sources other than egg, milk, or lean beef as substitute reference proteins. A good quality soy-protein product might be considered as an alternative reference protein, but more comparative data from other investigators and laboratories would be required to examine this issue.

It was the recommendation of the group that a description of the reference protein used in metabolic studies should be given and based, in part, on results obtained with standard chemical and animal bioassay procedures. The importance of a reference protein in human metabolic studies is analagous to the use of a standard in analytical chemistry. However, this does not imply that concurrent studies with a reference protein are always necessary in each series of human metabolic experiments.

Energy requirements for adults and energy-protein relationships

The working group on energy requirements for adults and energy-protein relationships was asked to address the following major questions:

1. What is the effect of various factors on the digestion and absorption of dietary energy?
2. What is the consequence of energy deficits for population groups; of seasonal variation in energy requirements; and of adaptation to chronic or seasonal energy deficits?
3. What is the influence of dietary energy on protein metabolism and nitrogen balance?
4. What is the influence of dietary protein on energy metabolism and nitrogen balance?
5. What is the significance of protein-energy ratios of bulk, energy density, and the fat content of diets?

1. Host Effects

Genetic: It is impossible, in metabolic studies, to separate the effects of genetic and environmental factors on variation in nitrogen and energy absorption. It may be possible, however, by studying different populations under similar conditions, to obtain information on this point, although this is doubtful and has not been achieved to date. This comment applies to protein. When it comes to differences in digestible energy, there is little doubt that differences in lactose hydrolysis associated with differences in intestinal lactase activity have a genetic basis.

While the net effect on digestible energy is small, because lactase-deficient individuals are not likely to have milk as a major energy source in their diet, it would be prudent to be alert for other genetic differences in utilization of energy sources within or among different populations. The fact that low lactase levels can also be induced by environmental factors does not change the preceding argument. It does suggest, however, that, where milk is used as a sole source of protein in experimental studies, this factor should be considered in the interpretation of the data.

Intestinal parasites: Data were presented at the meeting (5) to suggest that mild-tomoderate infections with intestinal helminths have minimal or no detectable effects on nitrogen and energy digestion and absorption. Severe infections, however, do measurably reduce protein absorption, and in some populations where the burden of intestinal helminths is heavy this can have public health significance. A similar general statement cannot be made for intestinal protozoa. Those not associated with the production of diarrhea probably have little effect, although impaired absorption of nitrogen has been found with Giardia infections (M. Gupta, unpublished INCAP data).

The most important infections for most developing-country populations are those associated with acute and chronic diarrhoea. Since the effect is so variable, depending on the nature, frequency, and severity of the diarrhoea, it is difficult at present to give any quantitative estimates of the consequence of diarrhoea infections on nitrogen digestibility and absorption in actual "field" situations.

2. Energy Deficits in Population Groups

Appropriateness of dietary energy standards: It is not possible to make valid global recommendations for mean energy requirements. It must be assumed that, for adult populations who are maintaining body weight and composition, energy intake and energy expenditure are in balance in spite of wide variations in individual intakes. The consequences for pregnant and lactating women, however, may be lower birth weight babies that experience greater morbidity and mortality during infancy and reduced breastmilk output during lactation.

For adults and children an adaptation of great significance is a reduction in physical activity, although growth may also be affected. However, the observation that most populations in developing countries are consuming considerably less than current FAD/WHO estimated mean calorie requirements does not necessarily mean that they are deficient in calories. It may indicate that the current requirement estimations are too high, or that the individuals have been forced to reduce their physical exertion for work, recreation, or social organization.

The biological and social consequences of low energy intakes may be partly mitigated by metabolic alterations and by altering patterns of activity, both resulting in greater efficiency of utilization of dietary energy. To some extent, individuals or societies may have adapted to a lower availability of dietary energy, and a sudden increase in dietary energy would not necessarily be wholly beneficial. For example, it might lead to a greater prevalence of obesity.

Seasonal affects: Even though long-term adaptation to low dietary energy intakes may occur, as evidenced by survival of a population, this may conceal important seasonal effects. Under the conditions prevailing among lower socio-economic groups of a number of developing countries, individuals, particularly women, experience a significant loss of weight during the season of the year when food is most scarce and costly, and regain it when the harvest season arrives (6).

This has two particularly serious adverse consequences. First, women who are in late stages of pregnancy during the adverse season have infants with lower birth weights and higher infant morbidity and mortality. Second, there may also be an adverse effect on lactation performance. Also, periods of food shortage often come just at the time when there is a need for considerable energy expenditure in agricultural labour, hence a resulting weight loss. However, under experimental conditions, change in energy intake may have significant effects on nitrogen retention. It is clear that it is extremely important to adjust the energy intake of studies designed to determine protein requirements to one that is appropriate for the subjects and not associated with any long-range change in body weight or composition. Since the latter cannot be determined precisely in periods of less than a month, this means that definitive studies to establish protein requirements must be conducted over relatively long periods of time.

3. Effect of Dietary Protein on Energy Requirements

It is known that, with an energy intake that is borderline or adequate, an increase in protein intake can result in weight gain. The functional implications of this are not understood. It does appear, however, that energy requirements for maintenance of weight and body composition may be less when dietary protein is adequate.

4. Significance of Protein-Energy Ratios: Bulk, Energy Density, and Fat Content of Diets

The protein-energy ratio of a diet has been proposed as a means of evaluating the diet's ability to meet human protein needs when consumed at levels sufficient to meet energy requirements. Unfortunately, since energy requirements of individuals and populations depend on physical, biological, and social factors in the environment, no single set of protein-energy ratios can have general validity.

A further reason why use of protein-energy ratios in diets must be approached with great caution is the lack of any fixed association between relative protein and energy requirements. In fact, the environmental circumstances-physical, biological, and social-that require an adaptation to low dietary energy intakes are likely to be associated with factors such as infections, parasites, and low digestibility of diets that lead to increased protein requirements compared with those of more privileged populations. It is particularly hazardous to assume that protein-energy ratios calculated for populations have any significance for individuals because of this disassociation between energy and protein requirements.

It is still valuable to know the concentration of each in the diet relative to the amount consumed or consumable if the distribution of protein and energy requirements for a specific population is known. It will sometimes be evident that the percentage of protein relative to energy in a diet is grossly inadequate to meet protein needs of specified groups even if enough of the diet could be consumed to meet energy needs. This is particularly likely to occur for young children during periods of recovery from severe clinical malnutrition and/or infection, when the percentage of protein calories required is further increased (7). The low protein-energy ratios of diets consisting mainly of a cereal or cassava as the major energy source must be improved by either legumes or a source of animal protein.

5. Constraints Due to Dietary Bulk for Energy and/or Protein Density

It is not necessary to define or specify a protein-energy ratio in order to examine the adequacy to meet the needs of specific target groups of the protein and energy concentrations of diets relative to their bulk. However, it is necessary to determine whether enough of the diet can be consumed to meet energy needs and whether, if this is the case, protein needs are also met. It is not uncommon for underprivileged, vulnerable groups in the developing countries to be consuming habitual diets in which sheer bulk and energy density are constraints.

It is possible that when cassava, starch, or sugar becomes a major component of the diet, protein density is a constraint. Diets consisting almost entirely of cereals are likely to be inadequate in both protein and energy density. As indicated above, children recovering from severe malnutrition and/or infection are particularly vulnerable to such constraints, and it may often be necessary to add fat to the diet to provide sufficient energy density, or a more concentrated source of protein, or both. This means that an improvement in the quality and not just the quantity of the habitual diet is required.

Protein requirements for children

The working group on protein requirements for children was asked to address the following major questions:

1. An important factor in the utilization of food proteins, especially of plant compared with animal sources, is their digestibility. What differences in faecal nitrogen exist between populations with low protein intakes corresponding to those used to measure obligatory losses of requirement levels, and populations with habitual levels of protein intake from different food sources?

2. What is the significance of zero-balance intercepts; the use of nitrogen retention required for normal growth; and the use of integumentary losses in nitrogen-balance calculations?

3. What are the effects of acute and chronic infections and of other stress situations?

4. How do these affect catch-up growth?

Standardization of Methodology

The drafting group members were conscious of a number of limitations in the investigative approach used in the UNU-sponsored research and agreed that it should be supplemented by research following the guidelines for protein requirement studies on children devised by a 1977 FAO/WHO Expert Consultation (18).

Selection of Subjects

In principle, children should be representative of the general population from which they come, but this was rarely the case. At INCAP, they were all children who had previously been severely malnourished. The children who were studied in the Philippines were mostly mildly undernourished at the time of the study, the majority being below 90 per cent weight/height.

For future investigations it is recommended that the children selected for this type of study be representative of the segment of the population about whom there is concern. Children without obvious morbidity should be selected and, preferably, they should never have been severely malnourished. If, on initial selection, they are below 90 per cent weight/height, they should be rehabilitated for at least four weeks before the commencement of the study. Unpublished INCAP data show that it takes as long as 30 days for the creatinine-height indices to return to normal, even though weight/ height has achieved normality.

While frequently the investigators in the studies carried out so far had little option but to work with the subjects they did, in the future greater efforts might be made to obtain a more representative selection of the target population.

Energy Intake

Ideally, the customary energy intake of each individual child should be determined over a representative period of time, perhaps one month, and then the nitrogenbalance procedure should be carried out at that child's established intake. The standardization of energy intake levels used left much to be desired. In the studies carried out using the multiple protein level approach, either the energy intake was fixed at the 1973 WHO/FAD theoretical average requirement for that age or it was ad libitum based on fixed protein-to-energy ratios. In this latter situation, children who had low energy intakes also had low protein intakes.

We must recognize that these inconsistencies represent a shortcoming of experimental design. In the studies by Intengan, for example, the energy intakes were up to 10-20 per cent above the assumed physiological requirement because the ad libitum intakes were measured during recovery from mild to moderate malnutrition. The data must be interpreted in the light of these facts. In spite of this, however, it must be recognized that the INCAP team observed that a 10 per cent energy intake reduction at a fixed protein intake below the WHO/FAD safe level did not affect nitrogen balance in children. The same would appear to be true of the studies carried out by Tontisirin.

Energy Content of Food

Another potential source of error is the assumed energy content of food. It may be inadequate to use food composition tables to define the energy content of the diet, particularly for those based on traditional foods. What is important is the available energy content of food. It is recommended that in future studies the energy content of food and faeces should be measured directly by bomb calorimetry. If necessary, suitably prepared samples should be sent to a regional reference laboratory for this purpose.

General Health Status

The UNU collaborative study represents a mixture of children. Some were infested with intestinal parasites, although usually only mildly or moderately so. The experience of Ju, as described at the meeting, has clearly been that a low level of Ascaris and Trichuris infestation does not affect nitrogen balance. Even though infections with these worms are endemic to most developing countries, it appears unnecessary to deworm such subjects, since this would not significantly affect requirements. The influence of Giardia on nitrogen balance, however, deserves more detailed study. Apart from worm infestations, the UNU research subjects were apparently free of clinically manifest signs of infection that might have influenced the validity of the resuIts.

Protein Characteristics of the Dietary Proteins Tested

In some of the studies presented, information was not given on the amino acid composition of the diets used. Such information should be obtained, and this would facilitate comparisons among the studies from the different research centres. Food table values for amino acid compositions are rarely adequate, and it is recommended that in future studies of this type a reference laboratory should be available for the conduct of amino acid analyses. In the subsequent published accounts of the present studies a concerted attempt should be made to make amino acid data available for comparative purposes, in spite of the difficulties and limitations involved.

Physical Activity

Physical activity can also influence the efficiency of dietary nitrogen utilization. Energy output should therefore be standardized. Play facilities should be provided during the investigation and the child should be encouraged to use them. The use of "metabolic beds" should therefore be avoided whenever possible. One or two studies in the UNU project could have been influenced by a lack of attention to this detail.

Number of Levels of Protein to Be Fed for Balance Studies

The drafting group was concerned about the statistical procedures adopted for the analysis of the children's nitrogen-balance regressions. While the pooled regression analysis gives an adequate estimate of the mean nitrogen intake needed for a given level of balance, it does not provide a precise estimate of variation in requirements between individuals. We recommend that the present data be recalculated using regressions for individual children and that future studies be planned in such a way that they can be analysed on this basis.

The use of individual rather than pooled regression analysis necessitates at least four and preferably more levels of nitrogen intake. These should be fed around the estimated level for normal growth plus and minus 20 per cent. Lower or higher intakes would serve no practical purpose.

It was considered premature to make any comments on nitrogen requirements either on the apparent mean or on variance until the data are supplemented with those from additional studies under way and then reanalysed. However, there appears to be a remarkable similarity among most of the data from the different centres.

Integumental Nitrogen Losses

Such information on integumental nitrogen losses is essential for the true interpretation of nitrogenbalance data. The UNU data present, for the first time, nitrogen balance information on children between one and three years of age from two cultures, Taiwan and Guatemala. These studies were done under conditions where there was no overt sweating. With protein intakes of 1.4-3 g/kg/day, integumental losses were virtually the same (6-9 mg N/kg/day). Interestingly, and confirming previous adult findings, lower protein intakes yielded slightly lower integumental losses. With 0.5 9 protein/kg/day, it was 6-7 mg N, and with a nitrogen free diet it was 5 mg N/kg/day. It is recommended, in the interpretation of nitrogen-balance studies on children who are not sweating, that 8 mg N/kg/day be incorporated into the calculation of nitrogen balance. For studies carried out under circumstances where environmental temperatures are such that sweating is more profuse, the extra integumental nitrogen losses are unlikely to produce a significant error in the balance calculations.

Exclusion of Anomalous Data

The decision to use individual regression equations will ensure the detection of individuals producing anomalous patterns of nitrogen retention relative to intake. When the results are biologically unrealistic (for example, a negative regression coefficient) for the relationship between nitrogen intake and balance, the data for that individual should be discarded. In less clear-cut cases, it is recommended that objective decisions be made based on accepted statistical methods. If it is possible to repeat the nitrogen study on a given individual, this should be done.

While the exclusion of data always represents a difficult decision, it is essential to deal with this problem so that the calculation of requirements does not result in unrealistically high values. When data have been excluded in the calculation of nitrogen requirements for the pooled multi-centre studies, this should be clearly stated and the specific reasons given.

Zero-Balance Intercept and Growth

For the non-pregnant, non-lactating adult the zero-balance intercept (Bo), after taking into account the integumental losses, can be used as an indicator of the mean nitrogen requirements. In the case of the growing child, the adequate level of nitrogen intake should be one that allows the child to grow at an acceptable rate.

It was recommended that the present data be analysed by the individual regression approach to produce two values, Bo, the nitrogen for maintenance nitrogen balance, and Bg, the nitrogen intake to allow for daily growth corresponding to the mean annual growth rate at the 50th centile for a given size. Bo is largely of academic interest, but on a per kilogram basis the data would seem to indicate that it is the same for children as adults. For population groups, the relevant value for children is Bg.

At the level of the individual, however, growth, even in healthy children, is by no means a uniform process (7). Variations in growth rate up to five times the 50th centile are commonplace. At these times, more protein would be needed. It is impossible, at the present time, to predict exactly how much more is needed since changes in physiological efficiency are a distinct possibility. Furthermore, this variable growth rate limits the value of protein requirement estimates based on data observed from short-term nitrogen balance studies.

Valuable data would accrue if healthy children in different countries were followed longitudinally to determine precisely the natural fluctuations in growth and the extent to which they are paralleled by fluctuations in food intake. Special attention should also be placed on the voluntary selection of foods and the resulting different nutrient intakes to see whether or not there is a "hunger" for individual nutrients as well as for energy.

Determination of Obligatory Nitrogen Loss in Children

Three studies were presented at the meeting concerning obligatory nitrogen losses on diets containing very low amounts of protein. There was good agreement as to faecal nitrogen losses, but a discrepancy in the urinary nitrogen. The two INCAP studies suggested 34 mg N/kg/day as the obligatory loss, whereas the Taiwan data suggested 54 mg N/kg/day. A possible explanation lies in methodological differences; the diets in the Taiwan study provided 12-28 mg N/kg/day, whereas the INCAP diets were virtually nitrogen-free. Another possible explanation was that the Taiwan data were based on pooled collections covering days four to ten, whereas the daily analyses performed in the INCAP studies suggested that day four was too early to be included in the calculation of obligatory nitrogen losses.

Regardless of this unresolved problem, we do not recommend that new studies be initiated. Obligatory nitrogen losses are of value for calculating protein requirements using the factorial approach and for estimating true digestibility and BV data for protein foods, but are not needed for requirement estimates based on the zero-balance intercept approach. Moreover, ethical problems make further studies of this type undesirable, even though there were no ill effects to the subjects as a consequence of the low-protein intake in the studies presented.

Suggestions for Future Investigative Approaches

Laboratory and metabolic ward approaches are invaluable, but are inevitably of relatively short-term duration and can never accurately reproduce normal living circumstances. To be truly sure that a given level of energy or a nutrient is adequate, long-term studies are essential.

Two approaches suggest themselves. One would be on free-living children for whom food intake would be measured sequentially over an extended period of time in conjunction with measurement of growth, body composition, function, and basic well-being. The aim would be to determine, under prevailing circumstances, the level and quality of food that is compatible with health and with appropriate physiological and psychological performance. This approach cannot identify minimum requirements. In certain circumstances, food intake could be approached by relevant modifications of intake.

The second approach is a natural extension and would apply to circumstances where one had a more complete control over children's food intake, such as in child welfare institutions. Here apparent safe levels for short-term metabolic studies could be introduced and tested on a long-term basis. As an alternative to multilevel studies in a few individuals, a single level of dietary protein intake considered adequate could be given to a large number of individuals to observe the distribution of their nitrogenbalance response. If appropriate for most normal individuals, negative nitrogen balance responses should be rare but might occur occasionally.

The drafting group suggests that relevant indicators of overall health and well-being in studies of dietary protein adequacy should include:

(a) weight and height growth;
(b) assessments of lean body mass and adiposity, using techniques appropriate to technical facilities available; and
(c) the immune response.

Energy requirements for children and energy-protein relationships

The working group on energy requirements for children and energy-protein relationships was asked to address the following major questions:

1. What is the effect of various factors on the digestion and absorption of dietary energy?
2. What is the consequence of energy deficits for population groups; of seasonal variation in energy requirements; and of adaptation to chronic or seasonal energy deficits?
3. What is the influence of dietary energy on protein metabolism and nitrogen balance?
4. What is the influence of dietary protein on energy metabolism and nitrogen balance?
5. What is the significance of protein-energy ratios of bulk, energy density, and the fat content of diets?

The Energy Requirement of Children

1. The evidence from recent studies in Thailand and at INCAP shows that, by the classical criteria of weight gain and nitrogen balance, a net intake (measured by bomb calorimetry) of about 90 kcal/kg is adequate for children 2-3 years old.

It appears from these studies that net intake, determined by bomb calorimetry, is about 10 per cent lower than the calculated intake based on the Atwater factors (see table 1). If the FAD/WHO (8) estimated requirement of 101 kcal/kg at 1-3 years is reduced by 10 per cent, it becomes identical with the figure of 90 kcal/kg obtained by direct measurement. The consideration of net energy intake is essential if one is to compare energy intake with expenditure. When comparisons of energy intake are being made with requirement recommendation figures, or with other energy intake figures, both should be expressed in the same terms, that is, both based on Atwater factors. However, further work is needed on the comparison of conventional measurements of intake with those obtained by bomb calorimetry of food and faeces.

2. The criteria used for estimating energy requirements need to be critically reviewed. "Adequate" growth is usually assessed by reference to western standards. These may be inappropriate, not so much because of possible genetic variations in growth potential but because the average western child could be somewhat overweight.

Even in the most carefully conducted trials, the relation between nitrogen retention and weight gain appears to be quite variable. This can be explained partly by variations in the amount of fat and lean tissue deposited. It has been shown that children on the same diet do differ in the composition of tissue laid down (9). As a result, the expectation expressed at the 1977 FAD/WHO (8) meeting, that nitrogen balance might be the most sensitive criterion of the adequacy of energy intake, seems not to be substantiated by these findings.

TABLE 1. Energy Requirements and Nitrogen Balance: Mean Daily Protein and Energy Intakes

Protein (g/kg/day)

Theoretical intake: 1.75 Actual intake: 1.73 Absorbed:* 1.14

Energy (kcal/kg/day)

Theoretical intake   120 110 100 92 83
Gross intake**   118 106 99 91 81
Net intake***   106 96 90 82 71

Source: B. Tord F. Viteri, unpublished INCAP data, 1980.
0 Coefficients of variability between 3 and 5 per cent.
* "True" N digestibility = 66 9 per cent.
** Gross intake measure by bomb calorimetry.
*** Net intake = gross intake-faecal energy (bomb calorimetry).

There also seems to be little justification for the suggestion (3) that for nitrogen retention to be considered "adequate" in children 1-3 years old it should be at least 70 mg/kg/day. The expected retention for growth at this age would be more nearly in the range of 15-25 mg/kg/day. Substantial variation from day to day is to be expected; what matters is that the average retention over a period should reach the level indicated.

3. Almost important criterion of the adequacy of energy intake is that it should support a "satisfactory" level of physical activity. There is evidence from one sutdy (INCAP) that the initial response to a fall in energy intake is a decrease in expenditure rather than in growth or nitrogen retention. Physical activity promotes not only skeletal growth but also interaction with the environment and hence stimulates mental development. Estimates of physical activity are not easy when it is measured, and the definition of what is "satisfactory" must be subjective. Nevertheless, observations of physical activity should be regarded as essential in all future studies of this kind, and a decrease in physical activity below "normal" should be avoided.

4. The rate of linear growth is, for many purposes, a better measure of the nutritional state of young children than the rate of gain in body weight. This criterion should be used whenever possible in future studies of the adequacy of energy intakes, but a longer period of observation will be necessary and it must be certain that protein is not a limiting factor. Thought needs to be given to other possible criteria, particularly those that measure outcome over an extended period.

5. It is clear from measurements of food intake that throughout the third world the energy intakes of young children frequently fall below the estimated requirement. A common estimated intake would be 75 kcal/kg/day (calculated), representing a deficit of about 25 per cent. The most obvious manifestations of this deficit are reductions in weight for height and in physical activity.

A commonly observed pattern of change in developing-country populations is that growth in weight-forheight begins to fall at 3-6 months, reaches a minimum at 12-18 months, and then returns toward normal by three years, leaving a child who is stunted but not necessarily underweight.

Weight for height is usually assessed in relation to western standards, and some percentage of the median standard is commonly taken as a cut-off point separating those who require action ("malnourished") from those who do not require action ("normal" or mildly undernourished). A cut-off point of this kind needs to be related to measures of risk-of death, morbidity, or impairment of function, A start has been made in several centres on the assessment of risk, but much more needs to be done. When weight deficits are being related to morbidity, it is essential to separate children into age groups, because the risks associated with a given deficit vary with age.

6. In all parts of the world there appear to be seasonal variations in growth. In poor countries these may be attributed to variations in food intake and in disease transmission; in rich countries the cause is not clear. It may, perhaps, be a difference in the level of physical activity. These seasonal effects must obviously be taken into account in comparative studies.

7. One of the most important questions for the future is the significance of a child's adaptation to deficits in energy intake. Adaptation is difficult to define, and this term has been used with a number of different meanings. Nevertheless, the general concept is an essential component of modern thinking in biology and nutrition.

One form of adaptation to shortage in food supply is a decrease in growth. It has been suggested, for example, that stunting is an adaptive change. Another is a decrease in physical activity. A third is a change in the efficiency of the utilization of food for metabolic and mechanical work. In all these cases the balance of advantage and disadvantage of the adaptive change to the well-being of the individual should be considered.

Energy-Protein Relationship

Energy and protein metabolism are closely interrelated. Several short-term (10-day) studies have shown that the intake of protein for zero nitrogen retention decreases with increasing energy intake, not only when the starting level is at deficient energy intake levels but also when intake reaches excess levels. A long-term study in Thailand (40 days) failed to show a decrease of nitrogen retention with decreasing energy intakes to levels considered 10 per cent below requirements and associated with lower energy expenditure and rate of weight gain. It would appear from present evidence that long-term studies are warranted that are based on energy intake and activity level immediately preceding the study.

On the other hand, a reduction of protein intake while energy intake remains constant can reduce the rate of growth in terms of weight and height even when nitrogen balance is not negative. The mechanisms for this effect are not clear. Apart from the specific dynamic action of proteins, a high protein intake does not appear to affect energy requirements.

Effects of Energy Intake on Physical Activity and Growth

Apathy and low physical activity have been observed in children of populations where energy deficiency is prevalent. Recently, quantitative estimates of physical activity and energy expenditure of children on energy intakes below estimated requirements have shown proportional decrements in the activity component of energy expenditure.

Moreover, such decrement takes place rapidly (within a week) in one- to three-year" old children when energy intake is reduced experimentally to levels slightly below estimated energy requirements. Energy conservation by a reduction in activity thus appears to be a response to deficient energy intakes in children as well as in adults.

Recent studies in animals and children in rapid growth phases and receiving sub optimal energy intakes have shown that a programme of enforced physical activity is associated with increased linear and lean body mass growth when compared with pair-fed but less active animals and children (10). These findings suggest that physical activity is necessary for adequate growth and that it enhances the efficiency of energy and/or protein utilization. They also point out the desirability of the maintenance of physical activity in children in metabolic studies aimed at exploring dietary energy protein interrelations, particularly when growth is considered a dependent variable. This has not been considered in most past studies.

Significance of Protein-Energy Ratios: Bulk, Energy Density, and Fat Contents of Diets

From all available evidence, a protein concentration above 7.5 per cent of calories when corrected for quality appears not to bring additional benefits to healthy children. For children recovering from protein energy malnutrition, infection, or other stress, this proportion should be higher, but probably need not be beyond 12 per cent. The lower limit for this value of corrected protein-energy intake should be above 5 per cent for healthy pre-school children. This should be kept in mind in attempts to increase the energy density of diets based on cereal-legume mixtures.

Studies on pre-school children fed five times a day on a free choice of corn and bean preparations common in their habitual diets have proven that these foods can be consumed in amounts that fulfil safe protein intakes, but that energy intake was inadequate and resulted in poor growth (weight) gains. An increase in fat calories from 8 per cent to near 20 per cent, and energy density from 4.5 to 4.9 kcals/g food (9 per cent increase), overcame both the energy intake deficit and the poor weight gains. Further addition of fat brought no additional improvement.

Addition of fat to infant and pre-school-child food preparations not only increases the energy density but also facilitates the swallowing of the solids and porridges that otherwise may be too gelatinous [agglutinated) for easy consumption by young children. This, and probably bulk, impair the capacity of cereal-legume mixtures, without fat added in appropriate amounts, to fulfil energy requirements.

Bulk-energy density-fat interrelationships in cereal-legume diets require very active research, including consideration of population beliefs and practices about infant feeding of such foods.

Infection and Catch-up Growth

Infection leads on the one hand to anorexia and decreased food intake, and on the other to losses of energy, nitrogen, and other body components. The extent of these changes is highly variable according to the nutritional status of the host and the severity and type of disease. In order to determine the effect of infections on the requirement for energy and nutrients, the magnitude of these losses must be known. In view of the range of variation, it will be difficult to draw realistic general conclusions from direct measurements on small numbers of children under closely controlled metabolic ward conditions.

A promising approach, which needs to be more widely pursued, is to establish the relationship under field conditions, and on a population basis, among the three variables: frequency, severity, and duration of the infection; food intake; and growth. It should then be possible to estimate the extent to which, on average, infections contribute to growth deficit, and hence to calculate the extra intake of energy and protein needed to make good the deficits, i.e., for catch-up. A beginning has been made with this kind of study in the Gambia, Peru, and Guatemala.

Catch-up

When one attempts to calculate the requirements for catch-up 17) two points emerge. First, relatively more protein is needed for weight gain (assuming normal balanced tissue) than for maintenance; therefore the protein-energy ratio in the diet needs to be somewhat higher than normal (the exact value will depend on the rate of catch-up aimed at). Second, catch-up growth obviously requires an increased intake of both protein and energy, but the increase is probably four to five times greater for protein than for energy. Quantitative estimates of the intakes needed for various rates of catch-up growth were tabulated in a previous UNU report 17). These estimates were based on the assumption that tissue of balanced composition is being laid down, and on observed values for the energy cost of weight gain 111). Studies on children recovering from malnutrition in hospital have shown that these estimates are realistic. For example, a net intake of 150 kcal and 3.5 9 protein/kg/day (P:E ratio about 10 per cent) will, support rates of weight gain of up to 10 g/kg/day.

In practice, the main difficulty in securing intakes adequate for catch-up growth is that even the child whose appetite is good may be physic ally unable to eat the necessary quantity of food. In this situation, the nutrient density of the food and the extent to which it is glutinous or easily swallowed become matters of great importance.

Research under metabolic ward conditions has been, and continues to be, essential in the efforts to define as accurately as possible protein and energy requirements and the mechanisms involved. Upon seclusion in metabolic wards, however, the inevitable changes that take place in living habits and very often in levels and type of energy and protein intakes, as well as the limits of time of study imposed by these conditions, make it very difficult to translate the data into "real-life, natural" conditions and into "safe levels of intake" for different population groups.

Research should be directed to develop techniques and evaluate methodology that would allow investigators to conduct field research in protein and energy nutrition as closely as possible to the accuracy and precision of metabolic ward conditions. This should allow the scientific community to obtain quantitative information on an adequate number of subjects under free-living conditions.

A series of population groups in different food and ambient ecological settings whose intakes are considered low could then be selected. A series of measurements could be made, aimed at defining their characteristics in terms of protein and energy nutrition. if the indicators used for this purpose indicate "normal population behaviour," one could try to identify populations with even greater intake deficits, if available.

In any case, the proof that energy and/or protein intakes are not limiting should be ascertained by means of nutrition interventions. The choice of indicators to detect the normal or abnormal behaviour of population groups is critical. Measurements of good health and adequate performance were proposed, such as rate of linear growth for age, lean body mass and muscle mass for age, low morbidity, milk production, birth weight, physical work capacity and fitness, and immune responses.

(introduction...)

References

The chemical energy in foodstuffs, manifested by the liberation of heat during combustion, is used primarily for doing work (internal and external work). External work is that performed by the body in its environment; internal work is mechanical and chemical Synthesis of compounds in reactions that would not proceed spontaneously, transport of ion against electrochemical gradients, etc.) In the steady state, i.e., when there is no change in chemical composition and body mass, all the internal work performed is dissipated as heat as prescribed by the first law of thermodynamics.

Energy utilization should be taken to mean the amount of work (external and internal) performed in or by the body by a unit change (decrease) in body energy. The latter change is equal to the heat output in thermal steady state. The relation between the two is subject to the restriction imposed by the second law of thermodynamics, which can be expressed as DH = G-TDS, where the entropy term, TDS, is almost always so small that it can be neglected. The change in Gibbs free energy, DG, is equal to the maximum work that can be harvested in the process. This amount of work can never be realized lit is the theoretical case where all processes proceed reversibly). The actual work performed is always less than the maximum work and depends on the degree of coupling that the body can make between the spontaneous chemical reactions and the work Synthesis. ion pumping, muscular contraction, etc.). The efficiency of the process is then given by the ratio of the actual work done to the maximum possible work.

Although the energy input to the body can always be measured, the total amount of work performed by the body cannot. Therefore, the efficiency of energy utilization cannot be measured. However, it is possible to imagine an experiment in which changes in efficiency can be measured. If measurements of energy expenditure are made on the same individual, during two situations identical in total work (i.e., a given "regime" or "programme"), then any change in energy expenditure directly reflects a change in efficiency of energy utilization.

References

1. "Tropical Jejunitis (Tropical Enteropathy): Morphology, Specificity," session 11 in l.H, Rosenberg and N.S. Scrimshaw, eds., "Malabsorption and Malnutrition," A.J. Clin. Nutr., 25: 1080-1102 (Oct.-Nov. 1972).

2. Consultative Group Meeting on Energy and Protein Requirements, "Recommendations by a Joint FAO/WHO Informal Gathering of Experts," Food and Nutrition (FAO), 1 (2): 11-19 (1975).

3. Energy and Protein Requirements: Report of a Joint FAO/WHO Ad Hoc Expert Committee, WHO Tech. Rep. Ser. 522 (World Health Organization, Geneva, 1973).

4. V.R. Young and N.S. Scrimshaw, "Nutrition Evaluation of Proteins and Protein Requirements," in M. Milner, N.S. Scrimshaw, and D.l.C. Wang, eds., Protein Resources and Technology (Avi Publishing Company,Westport, Conn., USA, 1978), pp. 136-173.

5. Jin Soon Ju, W.l. Hwang, T.G. Ryu, and S.H. Oh, "Protein Absorption of Adult Men with Intestinal Helminthic Parasites," pp.131-138 below.

6. R.G. Whitehead, "Infant Feeding Practices and the Development of Malnutrition in Rural Gambia," Food and Nutrition Bulletin, 1 (4): 36 41 (Aug. 1979).

7. F. E. Viteri, R.G. Whitehead, and V.R. Young, eds., Protein-Energy Requirements under Conditions Prevailing in Developing Countries: Current Knowledge and Research Needs (WHTR-1/UNUP-18, The United Nations University, Tokyo, 1979).

8. "Protein and Energy Requirements: A Joint FAO/WHO Memorandum-An Informal Consultation Held at the Food and Agriculture Organization of the United Nations, Rome, 1977,"Bul/. Wld. Hlth. Org., 57 (1): 65-79 (1979).

9. G.G. Graham, A. Cordano, R.M. Blizzard, and D.B. Cheek, "Infantile Malnutrition: Changes in Body Composition during Rehabilitation," Rediat Res., 3: 579-589 (1969).

10. B. Tor. Schutz, R. Bradfield, and F.E. Viteri, "Effect of Physical Activity upon Growth of Children Recovering from Protein-Calorie Malnutrition," in H. Koishi, Y. Yasumoto, K. Iwai, M. Kanamori, Y. Muto, and T. Oanaka, eds., The Tenth International Nutrition Congress (Victory-sha Press, Kyoto, Japan, 1976), pp. 247-249.

11. D.W. Spady, P.R. Payne, D. Picou, and J.C. Wateriow, "Energy Balance during Recovery from Mainutrition," Am. J. Clin. Nutr., 29: 1073-1088 (1976).