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close this bookActivity, Energy Expenditure and Energy Requirements of Infants and Children (International Dietary Energy Consultative Group - IDECG, 1989, 412 pages)
close this folderThe energy requirements of growth and catch-up growth
close this folder6. Catch-up growth
View the document(introductory text...)
View the document6.1. Nutritional determinants of catch-up growth
View the document6.2. Use of weight/increment in body fat
View the document6.3. Body composition during catch-up growth

(introductory text...)

If the concept of catch-up growth is that of accelerated weight gain, either to make up for faltering or to repair a deficit, then it is possible to define a spectrum of conditions for which the nutritional requirements must vary (Figure 1). In childhood, growth is the normal state, and a slowing of the rate of growth will result in a progressive falling away from the normal growth channel with time. As growth is canalised, a return to the original growth channel requires an acceleration in the rate of growth. By and large, the tissue deposited during the process of acceleration will have a composition that is essentially similar to that deposited during normal growth.


Figure 1. Growth and body composition are normally canalised, so that following a period during which growth has been delayed or weight has been lost, there is an acceleration in the rate of weight gain, catch-up growth. The nature of the tissue which should be deposited during catch-up growth is determined by the pattern of tissue lost. This pattern will be more unbalanced the greater the degree of weight loss.

At the other extreme is the repletion of tissue in an individual, adult or child, who has experienced a period of actual weight loss. The weight that has been lost will comprise of tissue which is not balanced. During the process of weight loss, there is a relative preservation of visceral tissues at the expense of muscle and adipose tissue. Thus, the requirements for repletion of tissues is unbalanced in relation to the requirements for normal growth or maintenance. The greater the deficit that has to be repaired, the more unbalanced is the tissue that needs to be regained. Therefore, one may conclude that if the losses are uneven between individuals, then the desirable gains need to be of variable composition. Hence any assessment of catch-up growth needs to take into consideration the composition of the tissue gained. My comments will focus upon catch-up growth in humans as measured by a rate of increase in weight that is substantially greater than the normal rate of weight gain at the corresponding chronological or developmental age. Although the focus will concentrate upon the energy requirements for catch-up in weight in young children recovering from severe undernutrition, the general principles do not appear to be different in situations such as catch-up in preterm infants, or in adults following stress or injury.

6.1. Nutritional determinants of catch-up growth

Up to 1961, the general impression was that the main determinant of the rate of catch-up weight gain should be the dietary intake of protein. However, based upon a series of balance studies, WATERLOW (1961) noted:

"The rate of weight gain depends more closely on the intake of calories than of protein within the range studied (100 to 200 kcal/kg per d, 2 to 7 g protein/kg per d). For 150 kcal/kg per d, a protein intake of 3 to 4 g/kg per d is adequate."

As growth represents an increment in the net energy content of the body, energy intake must exceed energy expenditure for tissue deposition to take place. Our interest is in the form in which the energy is deposited, the efficiency with which the deposition takes place and the effect of other specific nutrients upon the pattern of tissue deposition. Each consideration is intimately related to the other, and it is difficult to obtain a clear impression of the interrelationships, without considering them as isolated entities in the first instance.

A series of elegantly conducted experiments enabled ASHWORTH (1975) to define with some precision the detailed relationship between energy intake and the rate of catch-up weight. She was able to show that during catch-up growth the rate of weight gain might be 15 times as fast as that of normal children of the same age. The weight gain was associated with a high food intake. As the weight of the children approached that appropriate for their height, there was an abrupt and dramatic voluntary reduction in the food intake, which fell by 30%. In concert with the decreased intake of food, the rate of weight gain dropped to levels comparable with those of normal children of the same weight or length. Overall there was an increase in the efficiency of food utilisation during the catch-up period. As weight-for-height was reached, there was a tendency towards an increase in body fat. When the actual rates of weight gain were compared with the rate of weight gain predicted from the equations of MILLER and PAYNE (1963) there were major differences (ASHWORTH, 1969a). It could be shown that there was a highly significant relationship between the rate of weight gain and the increase in postprandial metabolic rate (BROOKE and ASHWORTH, 1972). The evidence appeared to suggest that the children were eating to satisfy a need for energy. When they were allowed ad libitum access to a high-energy milk preparation, they ingested 219 kcal/kg per day. With a lower energy density preparation offered ad libitum, although there was a voluntary increase in the volume of milk consumed, they were unable to achieve the same intake as on the denser diet, and the mean energy intake fell to 168 kcal/kg per day. After the children had achieved an appropriate weight for their height, they no longer consumed an increased volume when the lower energy milk preparation was offered. It has been suggested that the maximum intake of energy is of the order of four to five times BMR (PAYNE and JACOB, 1965). ASHWORTH (1969b) has shown that the standard metabolic rate of the children she studied was of the order of 50 kcal/kg per day; therefore a maximum intake of 219 kcal/kg per day is about 4.3 times BMR. The conclusion that children eat for calories during catch-up weight gain has its attractions, but has never been critically put to test.

6.2. Use of weight/increment in body fat

The advantage in exploring the protein requirements for weight gain is that the outcome indicator weight can be measured with considerable accuracy and reliability. However, the danger and disadvantage are that there is a tendency to assume that all weight gain has the same composition. This pitfall is often avoided for the relative proportions of lean and fat tissue gained, but the variability of lean tissue composition has not been as widely appreciated. Total body water has been used extensively as an index of lean tissue mass; the assumption being that the relationship between water and lean tissue is relatively invariant. PATRICK et al. (1978) have shown that, during the early phase of rapid weight gain, children recovering from severe malnutrition demonstrate a significant increase in the relative hydration of the body, which progressively tends towards the normal as recovery proceeds (Figure 2). Therefore, the use of total body water to derive values for lean body mass or fat mass is particularly liable to error during the early period of most rapid weight gain, although values derived from measurements of total body water may be of use when taken over the entire period of catch-up growth. This observation may explain why ASHWORTH found that the ratio of observed to theoretical weight gain was greater than 1 during early catch-up growth.


Figure 2. Total body water was measured in severely malnourished children on admission, while they were receiving a maintenance intake of energy and nutrients, and at times during recovery on a high-energy diet. Expressed as a percentage of body weight, body water was significantly greater in children with oedema (Kw+) than in the same children when they had lost their oedema (Kw-), or in children who had never had oedema (M). During early catch-up growth there was a significant increase in total body water as a percentage of body weight for all groups of children (RG1). Total body water tended towards normal as recovery proceeded, RG2, RG3, R (PATRICK et al., 1978).

6.3. Body composition during catch-up growth

Assessment of changes in body composition requires an assessment of the absolute or relative contributions of water, lean and adipose tissue to weight gain, with some indication of the degree of cellular hyperplasia or hypertrophy. Unfortunately, there are very few direct measures of body composition which can be applied with confidence during catch-up growth. One of the predominant changes during weight loss is a loss of muscle mass, which justifies efforts to measure muscle mass as directly as possible. A useful, but difficult approach, has been to measure muscle mass by following the dilution and kinetics of a tracer dose of 15N-creatine (PICOU et al., 1976). The method has been validated in laboratory animals for whom in vivo measurements of muscle mass correlated closely with cadaver analysis (REEDS and LOBLEY, 1990). Muscle mass was measured in severely malnourished children over the course of recovery. With the attainment of an appropriate weight for their height, the muscle mass of the children was approximately doubled (Table 2; REEDS et al., 1978). As the muscle mass represented an increasing proportion of body weight with recovery, this provided some confirmation of the clinical impression of disproportionate loss of muscle in the malnourished state. In order to identify the cellular basis of these changes, the DNA and non-collagen protein content of a muscle biopsy were measured. Using this information it was possible to calculate the number of muscle nuclei and the non-collagen protein to DNA ratio, the effective 'cell size'. There was no significant difference in the total DNA between the malnourished and recovered children, and the values fell around the middle of the expected range for normal children of the same height. In children in whom paired studies were carried out, a small increase in DNA was appropriate for the increase in height over the same period of time. There was an increase in the protein/DNA ratio with recovery of about 20%. However, even at recovery, the protein/DNA ratio was only about 60% of the ratio that would have been expected for a child of the same height. Therefore, although recovery, defined as the attainment of an appropriate weight-for-height, was complete, the muscle mass had not shown complete recovery, even at the cellular level.

Table 2. Muscle mass was determined in malnourished children and again after recovery, from the dilution of a tracer dose of 15N-creatine. The composition of the muscle was determined from a muscle biopsy (REEDS et al., 1978)


Malnourished

Recovered

Muscle mass (kg)

1.00

1.91

Muscle mass/body weight (%)

16

22

Muscle DNA (g)

2.05

2.38

Muscle non-collagen protein (g)

153

265

Non-collagen protein/DNA (g)

92

110

Similar conclusions have been reached using more indirect methods for assessing compositional changes. BROOKE and WHEELER (1976) found that skinfold thickness was up to 99% of normal by recovery, whereas arm muscle area and total body potassium, both indices of lean tissue mass, were 78% and 73% of normal, respectively. Therefore, in relation to a normal child of the same height, the children studied by BROOKE and WHEELER (1976) had a body composition with an excess of fat of up to 10% and a 10 to 15% deficit of lean tissue. On histological examination, the fibre size of clinically recovered subjects, age 13.8 months, was only 60% of that for a well-nourished 6-month-old (HANSEN-SMITH, PICOU and GOLDEN, 1979).

A somewhat different approach to assessing the nature of the tissue deposited during catch-up growth can be taken by a 'cost-of-growth' analysis (JACKSON, PICOU and REEDS, 1977). The energy available for deposition as new tissue is related to the weight of tissue gained. For any given quantity of energy deposited, adipose tissue with an energy density of 35 kJ/g will result in less weight being gained than lean tissue with an energy density of 5.6 kJ/g. The estimates of the energy cost of weight gain may vary from 35 to 14 for a range of different situations implying 0 to 53% of lean tissue accretion (FAO/WHO/UNU, 1985). An analysis of the energy content of the weight gained during catch-up would suggest that for many children the tissue deposited during catch-up growth tends to be relatively unbalanced, with a preponderance of adipose over lean tissue. This is the conclusion reached by Graham, having analysed the rate of recovery in a large series of children from Peru (MACLEEN and GRAHAM, 1980):

"The impressive gains in weight made by recovering malnourished infants are largely fat; reconstitution of lean tissue does not occur equally well at all rates of weight gain."

WHYTE, BAYLEY and SINCLAIR (1984) have reached a similar conclusion in their interpretation of the evidence relating weight gain in preterm infants to the intake of energy and protein: all studies show energy storage cost of growth (i.e., rate of accretion) much higher in low birthweight infants than in the fetus. Although KASHYAP et al. (1988) were able to demonstrate rates of weight gain and nitrogen retention equivalent to the intrauterine rate, the balance between energy and protein intake had to be very finely balanced. Protein tolerance appeared to be at its limit at optimal rates of accretion. Adults recovering from severe weight loss also appear to respond in a similar way, with a relative excess of adipose over lean tissue deposition, irrespective of the dietary protein intake (ELWYN et al., 1979). Similar observations have been made during recovery from anorexia nervosa (FORBES, KREIPE and LIPINSKI, 1984).