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Abstract
1. Historical work
2. Basal metabolism defined
3. Factors which may influence basal metabolism
4. Normative standards
Acknowledgments
References
Discussion (summarized by B. Schürch)
N.F. BUTTE *
* USDA/ARS Children's Nutrition
Research Center, Department of Pediatrics, Baylor College of Medicine, Texas Children's
Hospital, Houston, TX, U.S.A.
Extensive observations published in the early 1990s were used to derive normative standards for basal metabolism of infants. Because of practical considerations, the sleeping metabolic rate (SMR) has been used as a proxy for basal metabolism of infants. SMR, under most prevailing measurement conditions, represents energetic processes necessary for the maintenance of life, but also, to varying extents, the energy cost of growth, the thermic effect of feeding, and some body movement. In infancy, basal metabolism is accounted for primarily by the brain, liver, heart, and kidney. The decline in basal metabolism relative to body weight is secondary to the differential growth rates of these vital organs relative to muscle and fat. The basal metabolism of infants is roughly proportional to body weight, rather than to the fractional power of 0.75 identified for adults. In a series of observations on 105 infants, SMR was inversely related to body weight and parameters of body fatness. SMR differed by feeding mode, but not by age or sex. The parameters weight/length2, feeding mode and length, or weight, length, and feeding mode accounted for 78% of the variability in SMR. In a subset analysis, fat-free body mass did not augment the predictability of SMR. The advances in measurements of SMR have yet to account completely for the individual variability observed in the basal metabolism of infants.
The first investigation published on the gaseous metabolism of infants was conducted by FORSTER (1877) in Munich. The carbon dioxide production of 2 infants, one 14 and one 16 days of age, was measured in an open-circuit calorimeter. The apparatus was later used by RUBNER and HEUBNER (1898) in their classic studies of daily energy requirements of normal and atrophic infants. RUBNER (1883) pioneered studies on substrate oxidation and formalized the body surface area law, i.e., the theory that the metabolic rate per unit surface area is either the same for large and small animals or at least independent of body size. French scientists explored the effects of body surface area (RICHET, 1885) and of environmental and body temperatures on heat production (LANGLOIS, 1887). Infant metabolism (VO2 and VCO2) was studied simultaneously in Italy by MENSI (1894) and POPPI (1900), and in Czechoslovakia by SCHERER (1896) and BABAK (1901, 1902) using closed circuit calorimetry. A remarkable series of experiments was conducted by SCHLOSSMANN, OPPENHEIMER, and MURSCHHAUSER (1908) in Düsseldorf. These scientists recognized the importance of muscular repose and food intake in the measurement of basal metabolism.
In America, Atwater and Lusk initiated several investigations and HOWLAND (1911) made an important contribution by demonstrating the equivalence of direct and indirect calorimetry in infants. In his experiments the difference between the two methods ranged from -1% to 3%. A series of investigations of newborn, premature, and full-term infants was published by BENEDICT and TALBOT between 1914 and 1938. At Massachusetts General Hospital, they studied 37 infants, aged 1 day to 17 months, of varying nutritional states (BENEDICT and TALBOT, 1914).
Benedict challenged Rubner's surface
law; he concluded that basal metabolism was not determined by body weight or body surface
area, but by the active mass of protoplasmic tissue. In a subsequent series of studies,
Benedict examined the basal metabolism of 105 newborn infants (BENEDICT and TALBOT, 1915).
Minimum heat production averaged 42 kcal/kg/d for the newborn infants. In their most
extensive investigation, BENEDICT and TALBOT (1921) studied the minimal heat production of
73 infants from 8 days to 25 months. MURLIN and HOOBLER (1915) measured the heat
production of 10 infants, aged 2 to 12 months; it averaged 60 kcal/kg/d and was highest in
atrophic and underweight children and lowest in overweight children. Levine studied basal
metabolism and total energy requirements of normal and underweight infants with emphasis
on the influence of food, crying and muscular activity (LEVINE et al., 1927;
LEVINE, WILSON and GOTTSCHALL, 1928; LEVINE and MARPLES, 1931). CLAGETT and HATHAWAY
(1941) conducted a longitudinal study of 8 infants between 5 and 10 months of age.
Basal metabolism is the energy expended for cellular and tissue processes that ensure the maintenance of life. The basal metabolic rate (BMR) is measured under standard conditions in which the individual is at rest in a thermoneutral environment after a 12-to 18-hour fast (DUBOIS, 1936; BENEDICT, 1938). The resting metabolic rate (RMR) is measured under similar conditions, except that the individual is not fasted; measurements are generally made a few hours after a light meal (DURNIN and PASSMORE, 1967). Because infants are seldom quiet while awake, investigators have resorted to measuring the metabolic rate of sleeping infants. The sleeping metabolic rate (SMR) is defined as energy expenditure during sleep; investigators have not yet agreed upon definitions for such variables as the time since feeding, body movement, sleep stage, and duration of measurement. Some measurements have been made on fasted, sedated infants (KARLBERG, 1952), but most studies have been made on fed, sleeping infants (BENEDICT and TALBOT, 1921; TALBOT, 1925, 1938). Sleep and sedatives decrease BMR, and feeding increases it. Benedict attempted to assess the confounding effect of feeding on the measurement of basal metabolism. He measured energy expenditure 1, 2.5, 5, 9, 12, 18 and 21 hours after feeding and concluded that the effect was slight, if there was one at all (BENEDICT and TALBOT, 1914).
Basal metabolism of infants is accounted for primarily by the brain, liver, heart, and kidney (HOLLIDAY et al., 1967; HOLLIDAY, 1971, 1986) (Figure 1). Analysis of the BMR in relation to organ weight revealed that the BMR increased at a rate greater than that of organ weight during the intrauterine and postnatal periods. The increased BMR was attributed to increased enzymatic activity during the transition to extrauterine life. Thereafter, the metabolic activity of these vital organs was proportional to their increased mass; organ metabolic rate/kg organ weight was fairly constant from infancy to maturity (Figure 2). The pattern of growth of these organs in relation to the change in body weight paralleled the pattern of increase in BMR relative to the change in body weight (Figure 3).
The contribution of the brain to basal metabolism is exceptionally high in the newborn period (87%) and throughout the first year of life (53 to 64%) (HOLLIDAY, 1986) (Table 1). Two basic biochemical processes, protein synthesis and ion pumping, are estimated to account for 2/3 or more of basal metabolism (GRANDE, 1980). The energy consumed by the brain primarily supports active transport of ions to sustain and restore membrane potentials discharged during the process of excitation and conduction.
Table 1. Brain size and energy requirement relative to body weight and BMR at different stages of growth *
Body weight |
Brain weight |
Brain wt/body wt |
Brain MR |
BMR |
BrMR/BMR |
(kg) |
(g) |
(%) |
(kcal/d) |
(kcal/d) |
(%) |
1.1 |
190 |
17 |
- |
41 |
|
3.5 |
475 |
14 |
140 |
161 |
87 |
5.5 |
650 |
12 |
192 |
300 |
64 |
11.0 |
1045 |
10 |
311 |
590 |
53 |
* Adapted from HOLLIDAY, 1986.
The decline in basal metabolism relative to body weight is secondary to the differential in growth rates of organs with high metabolic rates (i.e., brain, liver, heart, and kidney) relative to those with lower metabolic rates (i.e., muscle and fat) (HOLLIDAY, 1971, 1986) (Table 2). Body composition is altered as growth proceeds. The weight of the brain, liver, heart, and kidney increases proportionally to body weight during the first year; the sum total of organ weights as a percentage of body weight remains relatively constant at 15% through infancy. Muscle mass increases from 20% in newborn to 23% in 1.5-year-old infants. Fat, although more variable, tends to increase from 12% at birth to 20% at 1.5 years.
Table 2. Body composition at different stages of growth *
Age (yr) |
Height (cm) |
Body weight (kg) |
% Body weight |
|||
Organ weight + |
Muscle mass |
Body fat |
ECF volume |
|||
Low birth wt |
1.1 |
21 |
< 10 |
3 |
50 |
|
Newborn |
50 |
3.5 |
18 |
20 |
12 |
40 |
0.25 |
60 |
5.5 |
15 |
22 |
11 |
32 |
1.5 |
80 |
11.0 |
14 |
23 |
20 |
26 |
* Adapted from HOLLIDAY, 1986.
+ sum of brain, liver, heart, and kidney.
In most studies of basal metabolism, its measurement has been related to some form of body weight measurement. RUBNER (1883) suggested that energy metabolism was proportional to body surface area. According to Rubner's law, the daily metabolic rate (in kcal) was equal to approximately 1000 times the number of square meters of surface area. This was found to be invalid for infants (BENEDICT and TALBOT, 1914, 1921; SINCLAIR, SCOPES and SILVERMAN, 1967). Subsequent investigators related basal metabolism to fractional powers of body weight.
KLEIBER (1947, 1975) investigated the relationship between metabolic rate (MR) and body weight (WT) as follows:
log (MR) = log (k) + n log (WT).
The linear correlation between the log MR and the log WT demonstrated that metabolic rate was proportional to a given power of body weight. The most suitable exponent for body weight in relation to energy metabolism was found to be 0.75 across several species. Under standard conditions the metabolic rate of adult homeotherms from mice to cattle was found to average 70 kcal per kg WT0.75 per day. Although infants were not included in Kleiber's investigations, this equation has been applied to infants.
Karlberg applied Kleiber's approach
of log-log analysis to his and other published data and found that basal metabolic rate of
infants was more or less proportional to body weight. Resultant exponents of body weight
were 0.918 (KARLBERG, 1952), 1.090 (BENEDICT and TALBOT, 1921), 1.113 (JANET and BOCHET,
1933), and 0.912 (BAER, 1929). Values differed significantly from Kleiber's 0.75. During
stages of rapid growth, the 0.75 derived from adult animals may not be appropriate for
infants. Energy expenditure for maintenance corresponds to energy which, according to
Kleiber, is related to the 0.75 power of weight. The exponent may be greater than 0.75 in
infants, because of the additional energy requirements for growth, or because of the
higher metabolic activity of adipose tissue in infants than in adults. The exponent tends
to fall as growth decreases in older children.
Age. There is no consensus as to the effect of age on basal metabolism, normalized by body weight, during the first years of life. The observations of BENEDICT and TALBOT (1921) indicated that basal metabolism (kcal/kg/d) increased during the first 12 to 18 months and thereafter decreased. In a longitudinal study by CLAGETT and HATHAWAY (1941), basal expenditure (per kg) was fairly constant for individuals throughout the series of observations. The data of KARLBERG (1952) indicated that BMR per kg body weight declined gradually in infants between 1 week and 1 year (Figure 4). All investigators stressed the pronounced variation among individual curves of basal metabolism vs age.
Sex. Sex has not been shown to be associated with effect differences in the basal metabolism of infants (BENEDICT and TALBOT, 1921; TALBOT, 1925).
Ethnicity. Ethnic differences in BMR, unrelated to nutritional status or possibly to climatic conditions, have not been demonstrated (FAO/WHO/UNU Expert Consultation, 1985). Little information is available on infants.
Undernutrition. The BMR of undernourished adults is believed to be depressed (KEYS et al., 1950); reports in the literature are less clear in regard to infants and children. Reduced metabolic rates have been reported in severely malnourished children (PARRA et al., 1973; BROOKE, COCKS and MARCH, 1974). This reduction appears consistent with clinical observations of hypothermia and, at the tissue level, the impairment of energy-producing mechanisms in muscle and of oxidative phosphorylation (WATERLOW and ALLEYNE, 1971). Contrasting reports of increased (BENEDICT and TALBOT, 1914; MURLIN and HOOBLER, 1915; LEVINE, WILSON and GOTTSCHALL, 1928; FLEMING and HUTCHISON, 1924) or normal (MONTGOMERY, 1962; KRIEGER and WHITTEN, 1969) metabolic rates may be the result of measurements made at different stages of recovery from malnutrition.
Food. Most measurements of the basal metabolism of infants have been confounded by the thermic effect of feeding (TEF), which many investigators have attempted to measure (HOWLAND, 1911; BENEDICT and TALBOT, 1921; MURLIN, 1925; LEVINE, 1927). Benedict estimated the TEF to be 8 to 15% above basal expenditure, but also noted the pronounced individuality of response. In his observations, which lasted up to 11 hours after feeding, the absolute minimum TEF was usually not found before 8 to 9 hours postprandially. The effect of the TEF on basal metabolism was dependent upon the size of the feeding; with a small feeding (about 50 kcal), measurements approached a basal level at the end of 4 hours.
Cold. Thermogenesis is stimulated in infants exposed to ambient temperatures below the critical temperature. BRUCK (1961) demonstrated that the metabolic rate of newly born, full-term infants can be increased by approximately 100% in response to cold.
Sleep. Energy expenditure declines with sleep and differs between the non-rapid eye movement (NREM) and rapid eye movement (REM) stages. Studies of infants have shown VO2 to increase by 16% (SCOPES and AHMED, 1966) and 9.4% (KAIRAM et al., 1979) in the transition from NREM to REM stages. Human growth hormone (hGH) is released during sleep (SASSIN et al., 1969). Spikes of hGH correlate with the development of NREM sleep. Because of the growth-stimulating action of hGH, measurements of SMR probably include the energy cost of growth.
Gestational duration and intrauterine growth. Basal metabolic rates of preterm infants are lower than those of full-term infants and increase at slower rates during the first month of extrauterine life. At thermoneutrality, metabolic rates of preterm infants (1000-2000 g, 2 to 31 days of age) did not exceed 40 kcal/kg/d (MESTYAN, JARAI and FEKETE, 1968). Because of their relatively large brain size and higher growth rates, oxygen consumption is higher in small-for-gestational-age (SGA) than in appropriate-for-gestational-age (AGA) preterm infants (SINCLAIR and SILVERMAN, 1964).