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Abstract
1. Introduction
2. A conceptual approach to defining desirable intakes in infancy
3. Childhood obesity and energy intake
4. Individual susceptibility to obesity
5. Desirable intakes in infancy5.1. Lower intakes on modern formulae
5.2. Differences in intake of bottle-fed and breast-fed children
5.3. Secular changes in intake of the breast-fed child6. Ambient temperature and diet-induced thermogenesis
7. Should energy requirements be based on data for breast-fed children?
8. The fat cell hypothesis
9. The Dutch famine study: An early programming of adiposity?
10. Links between childhood and adult obesity
11. Experimental findings
12. The effects of early feeding practices on the programming of metabolism
13. Infant growth rates and long-term survival
14. Conclusions
References
Discussion (summarized by W. Dietz)
W.P.T. JAMES and A. RALPH *
* Rowett Research Institute,
Greenburn Road, Aberdeen, AB2 9SB Scotland, U.K.
Infant nutrition in the 1970s was concerned with the high solute content of milk formula and its attendant risks of thirst, excess energy intake and infantile obesity. Campaigns encouraged a return to breast-feeding, and milk formulae were modified. The success of these campaigns has resulted in breast-fed children becoming less heavy even than children reared on newly formulated artificial milks. This raises the question of defining the optimal weight and height gain. Once these are defined, then new recommendations on intake can be developed. The intakes of breast-fed children cannot be used to define recommended intakes of formula since the energetic responses to the two seem to be different, and with so many differences in nutrient content, a comparison based only on energy intake is misleading.
Intakes of children differ by racial group, geographical area, time, season and social class, and there are substantial inter-individual variations in need. There is a tendency for excessive weight gain in obese families with below-normal intakes in obesity-prone infants and children. High intakes for a group of babies are associated with an increased prevalence of infantile adiposity.
The 1985 FAO/WHO/UNU allowances for energy in affluent societies could result in a 7% prevalence rate for obesity in children. There has been a secular decline in energy consumption in bottle-fed babies and in weaned children, but it is uncertain whether this is true of breast-fed babies. The secular decline in intake may reflect warmer homes and clothing and less physical activity than formerly. It is therefore difficult to specify appropriate energy intakes without taking into account physical activity, social and environmental factors, and individual susceptibility to weight gain.
If obesity is established in infancy or childhood, then there is now substantial evidence that this increases the probability of obesity in adolescence and in adult life. Experimental findings on baboons support a long-term programming of adiposity not mediated by an adipocyte hypercellular mechanism. This evidence supports a lowering of recommended intake in childhood. However, some data now suggest that rapid growth in infancy is advantageous on a long-term basis, thus casting doubt on the wisdom of accepting slower growth rates in breast-fed children. Early feeding practices, e.g., in relation to iron, fatty acid and cholesterol metabolism, also program long-term metabolism.
It is concluded that, given the uncertainty about the impact of different infant growth rates on adult risk of morbidity and mortality, a reduction in the recommended intakes for infants should only be undertaken when more reassuring data become available.
Traditionally, this topic was considered to be relatively uncontroversial. A dominant theme in nutrition during the early 1970s was the concern that babies, when fed artificially, were being given milk formulae with such a high solute content that thirst would lead to an excess consumption of energy and to infantile obesity. The 'bonny' fat baby of the postwar years came to be seen as a sign of inappropriate feeding.
The problem was later considered to be far more serious because of the popularization of the hypercellular theory of obesity. It proposed that overfeeding in infancy and early childhood would amplify the conversion of stem cells into adipocytes in the fat depots, so that an excess number of adipocytes was formed. Once this had been established during the early critical period in childhood when cell replication could occur, then adipocytes were fixed in number. This implied that adipocytes could not revert to stem cells nor be formed anew. Thus, the fixed and excessive number of adipocytes, each regulated to maintain a minimum amount of triglyceride, would lead inadvertently to a state of adiposity and metabolic sequelae, but with each adipocyte working normally.
These concerns accentuated the demand for a major reappraisal of the composition of milk formulae and led to a recognition that early artificial feeding should not be the norm. Huge campaigns in many countries were then developed to encourage a reversal to breast-feeding and a delay in the introduction of supplementary feeding.
So successful have these campaigns
been that elsewhere in these proceedings it will be shown that breast-fed children,
brought up with this new approach to child rearing, are less heavy and may be shorter than
children fed on even newly reformulated artificial milks. This once again raises the
question of how best to establish the optimal methods of feeding and the appropriate rate
of weight and height gain.
The now standard response to any analysis of requirements is to specify the end points so that one can identify the objectives. This is the "requirements for what?" argument. If it is first accepted that one needs to begin by defining growth patterns we should then establish whether the growth rates are appropriate or not. Only then can we work back to the original question and ask how much food is required to achieve these defined optimal growth patterns.
The analyses of the effects of different energy intakes must be considered from both the short- and long-term standpoint. In the short term, it seems difficult to define an upper limit to growth rates beyond which the baby or child suffers. If there is a maximum growth rate then there should be an upper limit to energy needs; overfeeding beyond this point leads either to the energy being dissipated as heat or to the excess energy being deposited as tissue; the child is then likely to become obese.
On a short-term basis, theromogenesis is unlikely to lead to problems of overheating, even in hot climates, and modest states of obesity are unlikely to be harmful. Only when a gross excess of fat and weight has accumulated will physical problems develop, e.g., genu valgum, disfiguring striae or eventually the Pickwickian syndrome of respiratory decompensation. Such a development takes several years of excess energy accumulation; so it is difficult to consider this type of information when assessing the short-term impact of excess energy and how to use this in developing values for the energy requirements of infants.
The longer-term effects of more
subtle changes in body composition, adiposity and metabolism are now receiving more
attention (see below). The issue of modest childhood obesity remains important, however,
because of the increasing evidence of a greater probability of adult obesity in those who
were overweight in childhood. An analysis of the relationship between energy intake and
childhood obesity is still therefore warranted.
One of the most interesting studies in young children comes from France where ROLLAND-CACHERA and her colleagues (1988) weighed the 5-day intake of 727 children aged 1-3 years. As in their previous study of 7- to 12-year-old children (ROLLAND-CACHERA and BELLISLE, 1986), they found no relationship between the degree of adiposity of the children and their measured energy intake. They defined obesity in terms of BMI which is a good approach in a group with such a limited age range. They then expressed the degree of excess weight in terms of the Z score of BMI. Whether the energy intake was specified in absolute terms or in relation to the child's height made no difference in the result. The most striking finding was the consistently higher energy intake of all the groups of children from working-class homes than of those from the professional and managerial classes. At each Z score level of BMI the working-class children showed a 4-16% higher intake than that of children from the professional and managerial classes. Not only was there no relationship between total intake and BMI, but there was also no relationship between corpulence and the intake of particular foods. The authors, not unreasonably, concluded that it was therefore difficult to specify appropriate upper levels of desirable intake on a population basis when individual susceptibility to adiposity seemed to be so important.
In theory it should be possible to encompass individual susceptibility by documenting the average energy intake of different populations with different prevalences of obesity and then defining the appropriate energy requirement as that associated with a low prevalence rate of obesity. Thus, in the same French study one can define an intake of about 5.5 MJ (1315 kcal) in the working-class children as being associated with a 6.3% prevalence of obesity whereas the intake of 5.2 MJ (1243 kcal) in the professional and managerial group was associated with a recorded prevalence rate of 2.8% only. Obesity in this instance was specified as a Z score of BMI above the 95th centile for the total population of children studied. A rate of 2.8% seems entirely acceptable, and one could therefore specify an energy requirement of 5.2 MJ (1243 kcal) for 1- to 3-year-olds.
For comparison, the energy allowance suggested by FAO/WHO/UNU in 1985 specified boys aged 1-2, 2-3 and 3-4 as needing 5.0, 5.9 and 6.5 MJ (1195, 1410 and 1554 kcal)/d, respectively, and girls 4.8, 5.5 and 6.0 MJ (1147, 1315 and 1434 kcal)/d. This therefore may average out as 5.6 MJ (1338 kcal) for the whole group of children from 1 to 4 years of age. This figure is a little above the energy intake of the French working-class children. If this crude analysis is continued and we assume that all French children were provided with the allowance recommended by FAO, then a prevalence rate for obesity of at least 7% could result, unless a very substantial proportion of children refused the extra food.
It should by now be clear that this approach is inappropriate because the whole argument neglects not only individual susceptibility but also other environmental and social issues which materially affect energy needs. Thus, we should be asking why the average working-class 1- to 3-year-old children in France are eating about 10% more than those children from the more wealthy families. It is inconceivable that the working-class children are storing the extra energy systematically on a daily basis, as a large proportion of the children would then become obese within months. Clearly, the children are physically more active and/or dissipating more energy under resting conditions, or the measurements are for some reason biased. These issues will be considered further below.
Additional evidence for the importance of environmental issues in relation to adiposity comes from Dietz's analysis of the National Health Examination Survey of Children in the United States (DIETZ and GORTMAKER, 1984). Dietz showed that the prevalence of obesity, assessed from triceps skinfold thicknesses, varied markedly around the United States with regional differences, seasonal effects and differences between urban and rural populations. These factors contributed a 2- to 3-fold variation in the prevalence of obesity in children aged 6-11 years. Thus, in the North-Eastern part of the United States there were 2 to 3 times as many obese children as in the West, large metropolitan areas had 50% more obese children than rural areas, and all regions showed a lower prevalence rate in the summer season.
When allowances were made for regional and seasonal differences and population density, it was still evident that white children had a 3-fold greater risk of obesity than black children. Clearly, racial factors could explain the last observation, but not the first three which might be related to differences in energy intake, physical activity, other environmental effects, or to dietary components other than energy. None of these were readily assessed, but on the basis of the French studies we would not expect to clarify the basis for the varying prevalence rates of obesity, even if monitoring of intake had been included.
More detailed longitudinal studies in the United States highlight the changing nature of the problem. Thus, in the Bogalusa Heart Study of 5- to 14-year-olds, measured repeatedly from 1973 to 1984, there is clear evidence of an increase in height of both white and black boys and girls and a marked secular increase in weight which amounts to a 0.5 kg average over the 11-year period of observation (SHEAR et al., 1988). Obesity, defined in this case in terms of a ponderal index of kg/m3 because of its better correlation with skinfolds and poor correlation with height showed an initial prevalence of 15% rising to 24% 11 years later. Detailed analysis, however, revealed that the greatest changes occurred in the 11- to 14-year-olds; so a faster rate of maturation could account for some of these findings. Nevertheless, those children above the 75th percentile for ponderal index showed a greater secular increase in weight than lighter ones. Either maturation was particularly accelerated in the heavier children or they have become even heavier in recent years.
Relevant to the present discussion is the finding that 24-hour dietary recall data of 10-year-olds showed no increase in energy intake despite this secular increase in weight and height. Durnin's studies of adolescents in Scotland also revealed that 11-year-old boys and girls studied over a 7-year period showed a modest increase in weight but a decline in intake which was presumed to be due to a secular reduction in physical activity. DURNIN et al. (1974) also found no relationship between the intake of a group of Scottish adolescents and their degree of adiposity.
DIETZ and GORTMAKER (1985) in the
United States have more recently shown that the prevalence of obesity increases with the
amount of time spent viewing television, but Durnin in Scotland found no discernible
differences between light and heavy adolescents when their physical activity was monitored
over a whole week. Part of the differences may relate to the relative dominance of
different factors in the aetiology of obesity in different societies, a point
re-emphasized by HARTZ and RIMM (1986) in their discussions of Danish data collected by
STUNKARD and his colleagues (1986) who sought to assess the importance of the environment
in determining obesity in either children or adults. Clearly, it is difficult to specify
appropriate energy intakes without taking account of the subjects' physical activity and
their individual susceptibility to weight gain.
The difficulties of specifying the upper desirable limits for avoiding obesity increase as one examines the literature on the more refined measures of energy turnover in childhood obesity. It is well recognized that obesity runs in families (GARN and CLARK, 1976), but this does not necessarily mean that the basis for this familial aggregation is genetic. Garn and his colleagues have made extensive analyses of the importance of educational, social and other factors in determining a child's adiposity, but these observations do not negate the contribution made by constitutional or genetic factors.
One of the first studies to consider the problem of energetics and childhood obesity was conducted on 4- to 5-year-old children in London (GRIFFITHS and PAYNE, 1976). In this and the authors subsequent study (GRIFFITHS, RIVERS and PAYNE, 1987), children of obese parents ate 20-22% less than children of normal-weight parents. Measures of total energy expenditure inferred from individually calibrated heart-rate studies showed that expenditure matched these intakes, and more direct measures of resting metabolic rate monitored 2-3 hours after a light meal showed it to be 15% lower in the children from obese families. Thus, Griffiths and Payne concluded that children from obese families with a recognized increased risk of developing obesity had a lower energy requirement than normal and that this related partly to their metabolism and perhaps to their spontaneous physical activity. On this basis, a child of an obese family will be overfeeding when consuming the average intake of the group.
Further evidence of this phenomenon comes from studies conducted even earlier in life in Cambridge, U.K. (ROBERTS et al., 1988). Using the D2O18 technique as well as direct measures of postprandial metabolic rates they observed that infants of overweight mothers in the first 3 months of life tended to have a lower postprandial metabolic rate but this was not statistically different from that of children of normal-weight mothers. The main difference was that, despite their energy intake being 13% less, those infants of overweight mothers who became progressively more overweight by 1 year of age had a total energy expenditure which was 21% lower than that of babies of lean mothers. The authors ascribe the genetic basis of the difference in energy metabolism to differences in spontaneous physical activity and present detailed calculations to justify this assertion. Yet, the observed differences in energy metabolism occurred at 3 months of age when one would not normally consider physical activity to be a major component of total energy output.
Studies conducted in Houston on 4-month-old babies fed either by bottle or breast showed that the energy cost of physical activity estimated from the difference between the measured metabolic rate and the total energy expenditure calculated from D2O18 amounted to only 27% of total energy output (BUTTE et al., 1989). There is, of course, some variation in this figure from child to child, but the average energy values amounted to 16 ±6 (SD) in breast-fed and 19 ±7 kcal/kg/d in formula-fed babies. By contrast, the Cambridge studies on 3-month olds had a difference between total energy expenditure and postprandial metabolic rate of 1.7 kcal/kg/d for the babies who became overweight and 12.4 kcal/kg/d for the lean group. These values may be underestimates if postprandial metabolic rates were not representative of 24-hour resting values, but nevertheless the Cambridge study implies an astonishing and surely readily observable lack of movement in the babies from overweight families who were gaining weight rapidly.
Bogardus and his colleagues (RAVUSSIN et al., 1988) also found that adult Pima Indians who put on weight tended to have a resting metabolic rate (RMR) below normal before weight gain. With the increase in weight, the RMR rose as would be predicted from the accumulation of lean as well as adipose tissue (JAMES et al., 1978). However, the reason why these individuals put on weight, having presumably had a reduced RMR for years, is obscure unless they became increasingly susceptible to obesity as their activity patterns or other habits changed in early adult life.
Despite concern for the validity of
analyses of the components of energy expenditure, it is reasonable to conclude that
obesity-prone children have below-normal energy requirements. Thus, when specifying an
average energy intake for a group of children we presuppose that each child regulates his
intake to meet his own energy needs. Preschool- and school-age children are probably
becoming less physically active, and this phenomenon together with the secular decline in
the age of puberty makes it increasingly difficult to specify even an average intake for a
group without considering a range of social and physiological issues.
5.1. Lower intakes on modern formulae
5.2. Differences in intake of bottle-fed and breast-fed children
5.3. Secular changes in intake of the breast-fed child
Other contributors will present
evidence on the total energy intake of breast-fed and bottle-fed children. The observed
differences have to be considered in three entirely different ways. Firstly, do the
differences between the nutrient content of the old and modern formulations of milk affect
intake? Secondly, are there intrinsic differences between the energy intake of children
fed by breast and bottle? Finally, has there been a secular decline in the energy intakes
of both breast-fed and bottle-fed children?
First, we need to consider the effects of new milk formulae on intakes: it seems to be accepted that the new formulations do lead to lower energy intakes (PRENTICE et al., 1988). This is often assumed to reflect the inability of children to adjust their appetite control systems and to consume an increased volume of formula, now that modern preparations are more dilute in their energy content. There is good evidence that intake is not totally controlled to maintain constant energy supplies, particularly in the first month of life (FOMON et al., 1969). Fomon, by manipulating the energy content of milk formulae, demonstrated that the capacity to adjust the volume became substantial and almost compensated for the different energy content of feeds after the first month of life. Calculations suggest that from 1 month of life the compensation amounted to at least 85% of that needed for a perfect maintenance of energy intake (JAMES, 1985).
This substantial but imperfect
regulatory mechanism has also been observed in many dilution experiments in adults (JAMES,
1985). Yet FOMON (1971) also showed that children could almost completely compensate by 4
months of age if volume dilution was the only factor tested. Similarly, when the fat and
carbohydrate content of the diet were altered, energy intakes remained the same (FOMON et
al., 1976). Thus, the direct physiological experiments of Fomon do not satisfactorily
explain the sustained differences of about 10% in intake between 4 and 9 months of age as
collated by Prentice for infants fed the old and modern formulae. Yet, PRENTICE et al.'s
1988 data include a very substantial amount of intake data originally collated and
analysed by WHITEHEAD, PAUL and COLE (1982), so there is little doubt that the differences
are genuine. Thus, some explanation other than energy dilution must be sought to explain
the lower intake on modern formulae.
The second question that is emerging is whether there are intrinsic differences in the intake of breast-fed and bottle-fed children. BUTTE and her colleagues (1989) are amassing evidence to this effect, fraught though the analysis is by methodological issues. The high intake of the bottle-fed child cannot be accounted for easily. The infant may find it easier to obtain milk in copious amounts from a bottle, the higher intake may depend on different feeding patterns instituted by the mother, the infant may eat more in response to unknown sensory stimuli in the formula, or there could be a metabolic appetite drive in response to a higher energy expenditure on the artificial formula.
There may well be a more flexible
response in energy expenditure to higher intake of energy in the first few months of life
when brown adipose tissue is more prevalent. This organ is noted for its thermogenic
activity and was invoked as one explanation for the propensity of some individuals to
obesity (JAMES and TRAYHURN, 1981). It now seems likely that this organ is too atrophic in
adult life to account for much thermogenesis (LEAN and JAMES, 1986). Nevertheless, its
activity could prove to be more responsive to formula than breast-feeding in early
childhood.
There is the intriguing question of whether there has been a genuine secular fall in energy intakes of both breast-fed and bottle-fed babies over the last 30 years. This issue has been one of the central questions being tackled by the Children's Nutrition Research Center in Houston and was also raised by the Cambridge group (PRENTICE et al., 1988).
There are many complications involved in using data on formula-feeding as an index of intrinsic changes in nutrient handling of babies over a period of decades. It would be much more convincing if breast-fed babies were now consuming less than formerly, although good data of babies almost totally breast-fed up to 6 months would be needed. Even this comparison might not be good enough if there were differences in the selection of women for study in the different periods.
LUCAS et al. (1987) have now provided new evidence on the energy intake of breast milk where the maternal delivery of milk was calculated indirectly using the D2O18 method for measuring energy expenditure. By adding to this value the presumed deposition of energy as the child grew, they estimated the total amount of energy consumed by the child. This new approach provided a low value for the apparent energy content of breast milk, i.e., 61 kcal/100 mL, the volume being calculated from the dilution rate of the deuterium label. The composite mean value given by many reviewers amounts to 70 kcal/100 mL (range 64 to 80 kcal/100 mL). Lucas argues that all previous studies are in error because the earlier estimates of energy intake were based on an excessive figure for the energy content of milk obtained from the breast by manual or artificial expression. Such milk may, particularly because hind-milk is included, have a higher fat content than normal.
If this conclusion is correct, it constitutes a substantial problem when trying to establish whether there have been significant changes in breast-milk energy intakes over a number of decades. The same energy value can be applied to the new as well as the old data on volume intake, but a higher volume intake might include more hind-milk with its higher fat content.
These arguments are set out in some
detail because it becomes increasingly clear that a simple analysis of secular trends in
intake, unrelated to different formula feeding, is difficult. Nevertheless, in the second
half of infancy feeding with milk formula remains common, and in the second year most of
the energy intake is derived from non-milk sources. WHITEHEAD, PAUL and COLE (1982) have
found an appreciable secular decline in energy intakes in children from 6 months onwards,
so an important environmental factor must be sought.
One such factor could be the increasing ambient temperature in houses with the advent of central heating. The effect of a higher ambient temperature could depend on both metabolic and behavioural factors. A higher temperature could make a child more soporific, thereby reducing physical activity, or it could reduce the resting metabolic rate. There is increasing evidence in adults that heat transfer through the abdomen after a meal affects the thermogenic response to a meal. Thus, wrapping an adult's abdomen to insulate it and reduce heat transfer has an appreciable effect by increasing the hepatic vein temperature and reducing total body oxygen consumption. If a similar effect is observed in infants, then environmental temperature could affect diet-induced thermogenesis, particularly if the baby's clothing was excessive.
It has also been recognized that environmental temperature has a profound effect on resting metabolic rate in the neonate (HULL, 1966), and this mechanism is considered to depend on the activation of brown adipose tissue (BAT). In the young infant such thermogenesis should not be discounted and in one study was particularly evident when fat was infused (SWYER et al., 1978). This fat-induced thermogenesis is consistent with the known substrates for BAT metabolism; experimentally the fatty acid content of the diet can modulate BAT function (MERGER and TRAYHURN, 1984).
Whether this can occur in newborn babies is unclear. However, Fomon, in further studies using modified milk-formulae with either a high carbohydrate or fat content, found not only that energy intakes were similar on formulae containing either 57% or 29% of the energy as fat, but that so were the rates of weight gain and growth in height (FOMON et al., 1976). Thus, the overall energetics of body maintenance and growth were not discernibly different on diets where the type of fat (58% corn and 42% coconut oils) was the same in the two preparations. This implies that at this early age the control of energy metabolism is not affected by the level of dietary fat. This conclusion has to be interpreted with caution, however, because in adults under carefully controlled calorimetric conditions, eating extra fat is less thermogenic than extra carbohydrate, and obesity-prone individuals may be less responsive than lean adults (JAMES, McNEILL and RALPH, 1990). Altering the fatty acid composition of the diet also alters the fasting respiratory quotient in adults for reasons which are as yet unclear (JONES and SCHOELLER, 1988).
We may conclude that if ambient
temperature does prove to be important, then there are further problems when specifying
the energy needs of babies in different countries where the ambient temperatures are
markedly different and where the effects of buildings, central heating and the cultural
differences in the approach to infant clothing may prove important.
Frequently, it is assumed that the breast-fed child provides the basis for specifying the normal needs for children in any society. Thus, the intakes of a breast-fed child are often considered the ideal. The fallacy of this approach is readily understood, however, if it is recognized that the purpose of deriving requirement figures is to specify the amount of food that a bottle-fed child can be expected to consume. Nobody knows how much the normal breast-fed child consumes and there is little concern provided the child is satisfied and grows 'appropriately'. The problem is how to specify the needs of artificially-fed babies. If they do consume more than the breast-fed, then we cannot use the breast-fed as the basis for standards, particularly if it is accepted that there might be metabolic differences in the handling of nutrients in the bottle-fed and breast-fed child. We then have to ask ourselves: what is the optimal intake of the bottle-fed child?
Recent evidence suggests that breast-fed children grow more slowly (i.e., 'less-well') than bottle-fed children from birth to one year of age. The slower rate of growth may not be an intrinsic feature of breast-feeding since classical data show breast-fed children in Europe or Africa growing faster than the NCHS standards. Even if growth is slower on breast feeding, it is often assumed that this slower growth must be satisfactory because, from a teleological point of view, evolutionary pressures will have led to the most appropriate pattern of breast-milk composition and infant response. This view is again unsound because the survival pressures are applied to both mother and child, and the child's ideal needs could be sacrificed in favour of reducing the drain on the mother. Furthermore, we need to ask whether slower or faster infantile growth rates are best for longevity and prolonged good health beyond the reproductive age where evolutionary pressures are not likely to exert much effect.
In the final section of this paper it is argued that evidence suggests that rapid infantile growth is advantageous on a long-term basis, thus casting doubt on the wisdom of automatically accepting the slower growth rates of the breast-fed child as optimal.
These arguments are the basis for
the present proposal that we approach the definition of upper desirable intakes by first
defining the optimal growth rates of infancy and then working back to see what intakes are
required with modern milk formulae to allow babies to grow at this newly-defined rate
under the particular climatic and cultural conditions being considered. First, we should
address the question of the long-term impact of early growth rates on adult adiposity.
The fat cell hypothesis of obesity (HIRSCH and KNITTLE, 1970) became extremely popular and led to the routine classification of patients in the United States as having either hypercellular or normocellular obesity. With the heavier adults usually having a longstanding history of obesity, often stemming from childhood, it was soon considered that the hypercellular grossly obese adults had been reprogrammed to generate new adipocytes and that this excessive proliferation occurred in childhood (KNITTLE, 1972). This concept was amplified by the observation that those obese children with an estimated high fat cell number had become obese in infancy (BROOK, LLOYD and WOLF, 1972). Infancy might then be a critical period for adipocyte development analogous to other critical periods of development.
Despite DAUNCEY and GAIRDNER's (1975) finding that the expansion of fat cells within the first year of life was ample for accommodating fat deposition without the need to invoke further replication of adipocytes, the enthusiasm for the hypercellular theory of obesity remained untouched until we showed from extensive studies of adipocytes in different depots that the true number of adipocytes in the body had been substantially underestimated. Once the numerous small adipocytes of the omentum and abdominal mesentery began to fill, the method of calculating total adipocyte numbers would imply spuriously that there had been an absolute increase in adipocytes (JUNG et al., 1978; GURR et al., 1982).
Since then, there has been very
little work on the hypothesis, but it should be recognized that criticism of the
hypercellular theory of obesity does not signify that early feeding does not affect adult
adiposity.
Much has been made of the observation that Dutch children whose mothers were restricted in food during the first and second trimester of pregnancy subsequently had a higher prevalence rate of obesity in early adult life. Conversely, children born to Dutch mothers whose food was restricted in the last trimester of pregnancy and the first 3-5 months of lactation had a reduced prevalence of adult obesity. The selective effects could be discriminated because the birth weights of children born during the German blockade of food supplies to the Dutch people had been carefully documented. On the basis of these findings, STEIN et al. (1975) proposed that prenatal and early postnatal influence had a long-term impact on adult adiposity.
While this may be true, there are other plausible explanations: the more overweight young women in Holland may have maintained their fertility for longer than normal; amenorrhoea developed in a large proportion of the semi-starved women of fertile age. Thus, there may have been selective conception by the more overweight women who could be expected to ovulate for longer when semi-starving. Their offspring, 20 or more years later, could then display the typical familiar aggregation of obesity which is recognized in most affluent societies. Thus, the Dutch famine study may not provide the most convincing evidence of the long-term effects of early nutrition on adult adiposity. Detailed studies of the Dutch adults for a variety of language, arithmetic, mechanical and other non-verbal tests failed to show any relationship to the time or length of famine during their prenatal or postnatal lives.