Human energy requirements: where are we now? Issues emerging from the 2001 Expert Consultation on Energy in Human Nutrition

P. SHETTY

Prakash Shetty is the Chief of FAO's Nutrition Planning, Assessment and Evaluation Service.

Scientific advances are being made in our understanding of the basis of human energy requirements. As technological advances enable us to obtain better and more accurate estimates of human energy needs, and as our appreciation of the problems associated with deficient and excess energy intakes leading to energy imbalance in humans grows, international agencies mandated to convene expert consultations in this area are confronted with changing scientific concepts and evidence as well as shifts in priorities of member countries' needs. This article explores two important developments - one technological and the other conceptual - that have shifted our understanding of energy balance in humans and hence contributed to changes in the approaches made by a recent expert consultation to review human energy requirements convened by FAO, the World Health Organization (WHO) and the United Nations University (UNU), at FAO headquarters in Rome.

It is useful in this context to provide a brief historical review of the conceptual shifts in this most important area of human energy needs, which will complement the historical outline of the nature of this consultative process reviewed in the article by Dr Weisell. The reports of the first two FAO Committees on Calorie Requirements (1950 and 1957) established general concepts, many of which have stood the test of time over the last half-century. The three important concepts established by these two forerunner expert committees were, first, that the energy needs of a group are represented by the average of the needs of individuals in that group. Second, that as far as possible, energy requirements should be determined from estimates of energy expenditure. The third generalization enunciated by these committees, relating to the concept of a "reference" man or woman, has, however, undergone modification over time. Although the concept of a reference man or woman was considered a convenient starting point for extrapolation and not intended to suggest an ideal standard, this concept has been relegated in most instances as being unduly restrictive with the recognition that both body size and physical activity patterns vary worldwide and undergo dramatic changes over time.

A major breakthrough in our ability to obtain reliable and accurate estimates of habitual energy expenditure was the application of the doubly-labelled water technique to humans under free-living conditions

The 1973 Report of the Joint FAO/WHO Ad Hoc Expert Committee on Energy and Protein Requirements reiterated statements that had been made in the past by expert groups that recommendations for nutrient requirements should be applied to groups and not to individuals. However, the 1973 report also made two additional important points: (a) that estimates of requirements are derived from individuals rather than groups; and (b) that the nutrient requirements of comparable individuals often vary.

The 1985 report was very clear in its statement that estimates of energy requirements should, as far as possible, be based on estimates of energy expenditure, since the prevailing method of determination - from observed intakes of food energy - was becoming unreliable and at the same time served to support a circular argument that access to food determined energy needs. The rationale for this conclusion was that both in developing and developed countries actual energy intakes are not necessarily those that either maintain a desirable body weight or provide for optimal levels of physical activity and hence health in its broadest sense. The experts at the 1985 consultation were aware of the limited data on energy expenditures, particularly among children. They were also conscious of the fact that no reli-able and widely usable method was available to the scientific and academic community to collect such data from a range of population groups worldwide.

When the Joint FAO/WHO/UNU Expert Consultation on Energy in Human Nutrition was convened in 2001 in Rome the situation related to the lack of data to arrive at realistic and evidence-based recommendations had dramatically changed. Almost all the recommendations that are likely to be made in the most recent report to be published later in the year 2002 will be based on reliable measurements of total energy expenditure obtained from infants, children, adolescents, adults and the elderly, as well as in special physiological states such as pregnancy and lactation.

Measurement of energy expenditure and its implication for estimating energy requirements

In the last two decades, major technolog-ical advances using stable (i.e. non-radioactive) isotopes have had a dramatic impact on the measurement of energy expenditures of free-living individuals in real-life situations. Estimates based on these measurements have replaced, to a large extent, the estimates using both direct and indirect calorimetry and the associated dependent methodologies such as heart rate monitoring, activity monitoring, pedometers and actometers. It is important to reiterate that these conventional methods continue to be important because the stable isotope technique measures cumulative total energy expenditure over a period of time and provides no accurate estimate of day-to-day variations or information relating to the nature and pattern of daily activities.

Doubly-labelled water technique

A major breakthrough in our ability to obtain reliable and accurate estimates of habitual energy expenditure was the application of the doubly-labelled water (DLW) technique to humans under free-living conditions.

This method was developed in the early 1950s by Lifson and McClintock (1966) to estimate the energy output of small ani-mals. During the first ten years of its use in humans, the DLW method was extensively validated and is now considered to be the "gold standard" for the measurement of total energy expenditure (TEE) of humans throughout the life cycle, from newborn infants to the very elderly. Although metabolic rate and the energy cost of different activities have been measured and daily energy expenditures of individuals computed from this in both developed and developing country settings, the measurement of habitual TEE by unrestrained, free-living individuals in real-life situations in their normal surroundings has had to await the use and validation of the DLW method.

The DLW technique for measuring TEE involves enriching the water within the body with the use of water labelled with a stable isotope of hydrogen (i.e. deuterium, ²H) and a stable isotope of oxygen (i.e. ¹⁸O). Following the administration of such doubly-labelled water, the manner in which these two isotopes are differentially washed out of the body over time is determined. The difference in the rate of excretion or washout of the isotopes from the body is a measure of the amount of carbon dioxide (CO₂) produced over that period of time (Figure 1) from which the oxygen consumption and hence energy expended over the same time period can be computed. The concentration of labelled hydrogen, i.e. deuterium (²H), decreases as a result of the dilution of the water in the body from unlabelled water consumed every day (in food and drink), by the addition of metabolic water produced as a result of oxidation of nutrients and by the loss of labelled water in urine, sweat and other excretions, and evaporative loss from the lungs. Deuter-ium is hence lost only in the water that moves through the body. Thus, the slope of the decay or loss of the deuterium in body water is a measure of water movement through the individual.

The process is slightly different for the stable isotope of oxygen (¹⁸O). Most of the labelled oxygen is lost as oxygen in the water molecule, but some is also lost as oxygen in the CO₂ molecule that is produced. Some of the labelled oxygen is seen in carbonic acid, or the bicarbonate formed by the dissolving of CO₂ in body water. The labelled oxygen, ¹⁸O, therefore disappears from the body through two pathways, i.e. in CO₂ and in water, unlike the single pathway of disappearance of the hydrogen isotope, ²H. Thus the slope of washout of ¹⁸O from the body is steeper than that for deuterium (see Figure 1). The differences in the washout slopes of ¹⁸O and ²H are a measure of the production of CO₂ over this period of time. This indirect measure of metabolic rate (indirect because hitherto it has been the convention to measure oxygen consumption by the body to estimate energy expenditure or heat production) may then be converted to units of heat production from estimates of the chemical composition of food being oxidized since the chemical composition of food determines the energy equivalent of each litre of CO₂ produced by the body as it expends energy.

The methodology using the DLW technique involves the administration of carefully weighed doses of ¹⁸O and deuterium to the subject followed by the collection of urine or saliva samples over time periods ranging from several days to several weeks depending on the rate at which the water moves through the body. For instance, in tropical climates, large amounts of water are consumed and excreted mostly as sweat, and hence the rate of movement or turn-over of water is much higher. In the early studies in temperate climates, samples were collected on a daily basis and analysed. However, it has since been shown that a minimum of two post-dose samples - one within hours of administration and the other at the end of several days or weeks - would suffice. Since the method of estimation of the isotopes in the sample using mass spectrometers is time-consuming and expensive, this represents an important saving in both costs and time. The specimens or samples are not radioactive, the stable isotopes do not decay over time and the samples are readily transportable as long as they are well sealed. These properties make it possible for specimens to be transported to countries where facilities exist to analyse the samples for isotopic enrichment. DLW thus has several advantages (summarized in Table 1) but it is important to recognize that the method also has limitations. The DLW technique is expensive as it requires the use of sophisticated equipment to estimate concentration of the isotope. In addition, there is a global shortage of ¹⁸O, which has driven its price beyond the reach of most investigators.

More effort to help developing countries with the DLW technology and other appropriate technologies was identified as a priority

The DLW technique of measuring TEE permits the determination of habitual free-living energy expenditure integrated over a period of days (usually between 7 and 20). The first data from humans were published in 1982 (Schoeller and van Santen, 1982). Between 1982 and 1994 sufficient data on TEE in human subjects were accumulated to form the basis for its use in arriving at energy requirements. A database of 1 614 DLW measurements from 1 156 individuals (aged 2 to 90 years) was collated and comprehensively analysed in 1995 (Black et al., 1996). The main analysis was made using a subset of 574 subjects for whom both TEEs by DLW and basal metabolic rate (BMR) measurements were available, under normal free-living conditions, although exclusively from subjects from affluent societies in the developed world. Three years after this compilation, it was estimated that the number of subjects on whom DLW measurements of TEE were available had tripled (Schoeller, 1999). The expert consultation of 2001 benefited for the first time from this large database of actual estimates of TEE throughout the life course, from infancy to adulthood and the elderly, using the DLW technique.

The number of studies carried out using the DLW technique in the developing countries is limited. A review by Coward (1998) provided an analysis of DLW data from 12 published papers. Since then there have been limited publications from the dev-eloping world, such as Kurpad, Borghona and Shetty (1997) and Borghona, Shetty and Kurpad (2000). These two latter studies address the issues that were raised by Coward (1998) when he lamented the lack of DLW data from well-nourished individuals in the developing world, largely as a result of the interest of investigators in taking measurements from the relatively poorly nourished labouring classes in the developing countries. It is evident that more data need to be generated in a systematic way from the developing countries if DLW estimates of TEE are to be used as the basis for arriving at energy requirements of adults worldwide.

Implications of DLW measurements for the recent expert consultation

The DLW technique is an important technological advance that is now considered the gold standard for the estimation of TEE. It provided the 2001 Expert Consultation on Energy in Human Nutrition with the enormous database of TEE measurements needed to arrive at evidence-based recommendations for human energy requirements, from newborn infants to the very elderly, and to assess the increased physiological needs during pregnancy and lactation. This recent consultation reiterated very strongly that energy requirement estimates need to be based on measurements of energy expenditure and not intakes. It reconfirmed the view that estimates of energy requirement refer to groups and not to the individual per se and that these recommendations for energy requirements of individuals are the mean of the group with no safe margin as with other nutrients. According to the 2001 consultation, the DLW method is accurate and should be the method of choice for estimating TEE; it should be used to validate the results obtained by other methods.

The current limitations relative to the cost and availability of ¹⁸O as well as lack of expertise and infrastructure to undertake DLW measurements, especially in developing countries, need to be addressed urgently. More effort to help developing countries with the DLW technology and other appropriate technologies was identified as a priority.

The 2001 consultation also made a strong plea that when DLW measurements are taken to assess TEE, information on the lifestyle and the pattern of activities over a day should also be recorded. The pattern and level of physical activities undertaken by individuals are important given the reductions in levels of activity both in the occupational and social spheres of urbanized modern lifestyles. These increasingly sedentary lifestyles are contributing to the problem of obesity in developed industrialized countries and are now also appearing in developing societies, particularly in urban settings.

The reported low energy intakes from food consumption studies conducted in developed and developing countries are now known to be unreliable and physiologically unsustainable

The data obtained by using the DLW method were considered a valuable resource for the estimation of the TEE of infants. Although this database was derived almost exclusively from studies in the developed world, the assumption that the requirements of infants for normal growth and development are the same worldwide provided the basis for energy recommendations for infants. Evidence had been emerging that the energy requirements of infants are lower than previously recommended, a view that was considered revolutionary in earlier consultations. However, evidence of TEE in infants based on DLW supports the view that energy requirements of infants needed to be lowered, as the 2001 consultation has now done.

Consideration of the concept of "adaptation" when estimating energy requirements

The 1981 expert consultation considered issues related to the concept of "adaptation" when estimating energy requirements to be important. This is evidenced by the number of pages devoted to this topic in the 1985 report, which provided a working definition of adaptation as: "a process by which a new or different steady state is reached in response to a change or difference in the intake of food and nutrients". The 1981 consultation had to wrestle with this concept largely because of the need to deal with the problem of variations in the energy intakes of individuals, both inter- and intra-individual. In addition, they were confronted with data from food consumption surveys that showed that individuals were living active lives on energy intakes that were considerably lower than those hitherto recommended on physiological grounds. The 1985 report considered both short- and long-term adaptations and made three general points with regard to adaptation: (i) that the concept of steady state was relative; (ii) that adaptations may be fundamentally of different kinds - metabolic, genetic and behavioural; and (iii) that adaptation implied a range of steady states and hence it was impossible to define a single point within the range that represented the "normal" state. The last general point implied that different adapted states will carry different advantages and penalties and hence the decision of what is "optimal" or preferable can only be made in the light of a value judgement. Clearly, this concept of a range of adapted states introduced a dilemma, since it follows that requirements cannot be specified on physiological grounds alone and may need to be based on value judgements made about what is considered desirable to achieve. The accumulation of considerable physiological and other scientific evidence in the interim period of nearly two decades has, however, resolved this issue such that the concept of adaptation is no longer considered significant when recommending energy requirements.

The concept of adaptation in energy metabolism arose out of evidence that the energy metabolism of individuals is variable and adaptable. Several publications had drawn attention to the possibility of such physiological variability in energy utilization between individuals. Norgan (1983) has, however, critically evaluated the evidence that was used to support the concept of adaptation in human energy metabolism and concluded that differences in body size and levels of physical activity may provide explanations for most of these observations. It was also shown that the principal response to a lowering of energy intake in adults depended on the previous nutritional status of the individual (Shetty, 1999).

In well-nourished adults, low energy intakes lead to the utilization of body tissue to meet energy needs and with a physiological response suggestive of increased metabolic efficiency. The reduction in body weight coupled with a small increase in efficiency will lower energy expenditure. Daily energy expenditure is lowered by a lower cost of physical activity, largely contributed by the reduction in body weight but also by reduced voluntary activity. There is little evidence of any improvement in the mechanical efficiency of work.

The response to marginal intakes or deficient diets in developing countries is compounded by an increased predisposition to infections and a generalized environmental deprivation. The effects of such undernutrition from birth through the developmental phases into adulthood are closely interlinked with both the immediate effects of childhood malnutrition and the evolution of adult undernutrition later in life. The principal response is a reduction in body size, which persists into adulthood as short stature, low body weight and a reduced muscle mass and fat stores. There is thus little evidence of an increase in metabolic efficiency or an enhanced mechanical efficiency of work in these individuals. Behavioural responses contribute to alterations in physical activity patterns and, along with the small body size, contribute much to reducing energy expenditure to balance the lower levels of intake. However, the compromised body size, altered physical activity patterns and reduced potential to carry out economically productive work have major costs - human and social - that the individual and society will have to bear.

The reported low energy intakes from food consumption studies conducted in developed and developing countries are now known to be unreliable and physiologically unsustainable.

The idea of costless adaptation was rejected with the recognition that there will always be a consequence to low energy intakes both in physical terms, i.e. low body weight, height or altered body composition, and in terms of compromises in physical activity

These low intakes are often just above or below the basal or resting energy levels and provide for nothing more than a day lying in bed. They are unlikely to reflect the true intakes of individuals who are leading an active life. DLW studies, when conducted in such supposedly low-intake individuals, have clearly shown that such intakes are unsustainable over the short (i.e. a few days) or the long (i.e. a few weeks) term without serious loss of body weight. The TEE estimates by DLW in these individuals provided evidence of serious underreporting of energy intakes (Goldberg and Black, 1998). This evidence has more or less settled the debate on whether adaptation can be considered a serious enough physiological mechanism to adjust to lowered energy intakes when individuals continue to maintain their body weights and habitual physical activity levels.

Implications of the concept of adaptation for the 2001 expert consultation

The dilemma that confronted the 1981 expert consultation when they had to wrestle with the concept of adaptation to variations in energy intake was not an issue at the expert consultation held at FAO in Rome in October 2001. The recent consultation was confronted with scientific evidence accumulated over the last 20 years, which indicated that while metabolic adaptation and improvements in metabolic efficiency may occur during energy restriction of individuals, this was of a trivial nature and could not form the basis for any alteration in an individual's requirements for energy. It was also observed that there were costs to this adaptation, which may manifest in an increased risk of infection and disease. The 2001 consultation recognized that while behavioural adaptation did in fact take place to a considerable extent, it was at a cost to the individual in terms of reductions in socially desirable activities. The costs to the individual and to society were compromises that should not be reflected in recommendations of energy requirements. Thus the question of adaptation that oc-cupied the minds of the expert consultation in 1981 was not an issue when the 2001 expert consultation deliberated on energy requirements 20 years on.

The idea of costless adaptation was rejected with the recognition that there will always be a consequence to low energy intakes both in physical terms, i.e. low body weight, height or altered body composition, and in terms of compromises in physical activity.

In conclusion, two examples have been used in this article to show how technological advances and the accumulation of good scientific evidence inform the debates of expert consultations and result in new reports from time to time - an essential normative function of United Nations agencies such as FAO to fulfil their mandate to the member countries.

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