(introductory text...)

Nancy F Butte

Children's Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine, Houston, Texas, USA

Descriptors: energy requirements, energy intake, energy expenditure, energy cost of growth, infancy

The Advisory Group of IDECG recommended that select parts of the 1985 FAO/WHO/UNU Report on energy and protein requirements be reviewed for possible revision and updating. The specific questions posed were:

1. Do the 1985 recommendations need to be revised: what are the main arguments for or against a revision ?
2. What would your recommendations be at this point in time?
3. What additional work would need to be done to resolve problems that persist in this area?

Energy requirements of infants based on energy intake

'The energy requirement of an individual is the level of energy intake from food that will balance energy expenditure when the individual has body size and body composition, and level of physical activity, consistent with long-term good health; and that will allow for the maintenance of economically necessary and socially desirable physical activity. In children the energy requirement includes the energy associated with the deposition of tissues at rates consistent with good health.' (FAO/WHO/UNU, 1985). This basic tenet set forth by the 1985 FAO/WHO/UNU Expert Consultation should be upheld.

Because it was not possible to specify with any confidence the allowance for a desirable level of physical activity, the 1985 FAO/WHO/UNU energy requirements from birth to 10 years were derived from the observed intakes of healthy infants and children growing normally. For infants energy requirements were based on energy intakes compiled by Whitehead et al (1981). Estimated energy requirements were set 5% higher than observed energy intakes to compensate for underestimation of intake (Table 1). Implicit in this approach is the assumption that ad libitum intakes reflect desirable intakes for infants. Although infant intake is largely self-regulated, it can be influenced by external factors.

Correspondence: NF Butte.

Compilation of energy intakes published before and after 1980

Whitehead et al (1981) compiled energy intakes of infants from the literature predating 1940 and up to 1980. The work represented 9046 data points during infancy, weighted to account for sample size. Analysis of the energy intake data revealed a highly significant curvilinear relation between energy intake per body weight in kg and age in months:

Energy intake (kcal/kg/d) = 120 - 10.4 age + 0.76 age²
r² = 0.41 (1)

The quadratic term was significant (P = 0.001). No differences were seen between sexes. The authors attributed the sharp fall in energy intake from O to 6 months of age to the rapidly decelerating velocity of growth, a reduction in the rate of fat storage, and a decrease in energy needed for maintenance per kg body weight. The rise in energy intake from 6 to 12 months of age was ascribed to the increase in physical activity as infants begin to crawl and then walk.

Because of possible secular trends in infant feeding practices, we examined energy intakes of presumably well-nourished infants reported after 1980. An analysis was performed on the mean energy intakes from 19 longitudinal or cross-sectional studies comprising 3574 data points (Table 2, Figures 1 and 2). As noted in Table 2, dietary methodology varied across studies.

Table 1 Energy requirements of infants from birth to l year (FAO/ WHO/UNU 1985)

	Total requirement
Age (months)	(kcal/kg/d)	Boys (kcal/d)	Girls (kcal/d)
0.5	124	470	445
1-2	116	550	505
2-3	109	610	545
3-4	103	655	590
4-5	99	695	630
5-6	96.5	730	670
6-7	95	765	720
7-8	94.5	810	750
8-9	95	855	800
9-10	99	925	865
10 11	100	970	905
11-12	104.5	1050	975

FIGURE 1 Mean energy intakes (kcal/d) of formula-fed, breast-fed and mixed-fed infants reported in 1982-1994.

FIGURE 2 Mean energy intakes (kcal/kg/d) of formula-fed, breast-fed and mixed-fed infants reported in 1982-1994

Weighed dietary records, dietary recall methods, or the test-weighing method for breast milk intake were used. Food intakes were converted to metabolizable energy intakes using food composition tables, or macro nutrients were analyzed and converted to gross or metabolizable energy using Atwater factors. Bomb calorimetry was used to measure the gross energy content of breast milk and formula in a few studies. Mean energy intakes as reported were used in the present analysis. Mean total energy intakes (inclusive of solids) of breast fed and formula-fed infants were weighted by sample size at each monthly interval yielding 107 weighted mean values used in the regression analysis (BMDP1R: Dixon, 1990). The multiple regressions of energy intake per kg body weight on age and age² are summarized below.

All: Energy intake (kcal/kg/d)

= 119 - 9.9 age + 0.82 age²
r² = 0.29; n = 107 (2)

BF: Energy intake (kcal/kg/d)

= 118 - 12.8 age + 0.89 age²
r² = 0.66; n = 59 (3)

FF: Energy intake (kcal/kg/d)

= 122 - 8.5 age + 0.73 age²
r² = 0.36; n = 48 (4)

Each of these three equations was tested against the earlier curvilinear equation published by Whitehead et al (1981). We do not have evidence for a strong secular trend in energy intakes of infants before and after 1980, since the regression coefficients did not differ significantly between the Whitehead and present databases. The ~ test for equality of the regression lines across feeding groups was significant, indicating differences in the relationship of energy intake and age between breast-fed and formula-fed infants (P = 0.001) (Figure 3).

Equations (2), (3) and (4) were derived from energy intake data as reported. Two technical problems with reported data arise in the case of the breast-fed infants. Breast milk intakes measured by the test-weighing method were corrected for insensible water loss (IWL) during the course of the measurement in a few studies only (Heinig et al, 1993; Michaelsen et al, 1994). The systematic negative bias caused by not correcting for IWL during, the test-weighing is well recognized: the difficulty has been to determine the magnitude of correction necessary to fairly represent the ranges of metabolic rates, ambient temperatures, humidities, and air circulation rates likely to be encountered. Rates of IWL measured by a number of investigators were as follows: 1.5g/kg/h, Levine et al (1929); 0.83g/kg/h, Kajtar et al (1976); 0.4-0.6 g/kg/h, Doyle & Sinclair (1982); 2.5 g/kg/h, Orr-Ewing & Heywood (1982); 1.9g/kg/h, Hendrikson et al (1985); 1.14 g/kg/h, Butte et al (1990b); 3 g/kg/h, Dewey et al (1991). Most of the measurements were performed under thermoneutral conditions. Levine et al (1929) noted that rates of weight loss may increase threefold above basal levels in temperatures sufficiently high to induce visible perspiration.

Table 2 Energy intakes of infants reported in the first year of life (kcal/kg/d). Mean ± s.d. (N)

Reference	Country	Design/Subjects	N	Type of food	Dietary method
McKillop & Durnin (1982)	Scotland	Cross-sectional Low-high SESa	162	formula solids	5d weighed record FCT, ME
Hofvander et al (1982)	Sweden	Cross-sectional	150	breast milk formula solids	1 d weighed record FCT, ME 0.75 kcal/ml
Dewey & Lönnerdal (1983)	U.S.A.	Longitudinal	20	breast milk solids	2 d weighed record, FCT, ME macronutrients 0.76 kcal/ml breast milk
Butte et al (1984)	U.S.A.	Longitudinal Middle SES	45	breast milk minimal solids	1 d weighed record bomb calorimetry GE 0.66 kcal/g breast milk
Dewey et al (1984)	U.S.A.	Longitudinal	12	breast milk solids	2 d weighed record, FCT, ME macronutrients 0.65 kcal/ml breast milk
Kohler et al (1984)	Sweden	Longitudinal Suburban	59	breast milk cow's formula soy formula solids	2 d weighed record 0.70 kcal/g breast milk
Martinez et al (1985)	U.S.A.	Cross-sectional Low-middle	442	formula solids	24h recall FCT, ME
Forsum & Sadurskis (1986)	Sweden	Longitudinal Middle SES	22	breast milk	1 d weighed record 0.67 kcal/g breast milk
Hoffmans et al (1986)	The Netherlands	Longitudinal	124	formula breast milk solids	24h recall test-weighing FCT, ME
Horst et al (1987)	The Netherlands	Cross-sectional	308	breast milk formula solids	24h recall test-weighing FCT, ME
Leung et al (1988)	Hong Kong	Longitudinal Low-middle SES	174	formula weaning foods	24h recall FCT, ME
Wood et al (1988)	U.S.A.	Longitudinal	22	breast milk	1 d weighed record bomb calorimetry GE 0.60 kcal/ml breast milk
Stuff & Nichols (1989)	U.S.A.	Longitudinal Middle SES	58	breast milk solids	5 d weighed record bomb calorimetry GE 0.65 kcal/g breast milk
Butte et al (1990b)	U.S.A.	Cross-sectional Middle SES	65	breast milk formula minimal solids	3 d weighed record 0.65 kcal/g breast milk GE
Butte et al (1990a)	U.S.A.	Cross-sectional Middle SES	40	breast milk formula minimal solids	5 d weighed record bomb calorimetry GE 0.64 kcal/g breast milk
Stuff et al (1991)	U.S.A.	Longitudinal Middle SES	40	formula solids	5 d weighed record FCT, ME
Sauve and Geggie (1991)	Canada	Longitudinal Low-high SES	114	formula solids	3 d food diaries FCT ME
Michaelsen et al (1994)	Denmark	Longitudinal	60	breast milk	1 d test-weighing; IWL macronutrients GE 0.72 kcal/ml breast milk
Heinig et al (1993)	USA	Longitudinal Middle SES	119	breast milk formula solids	4 d weighed record; IWL macronutrients GE 0.70 kcal/ml breast milk

Age (months)
1	2	3	4	5	6
			97.0 (71)
B-112 (25) F-120 (25)	108 (25) 107 (25)	96 (25) 101 (25)
113 ± 19 (17)	105 ± 25 (20)	93 ± 26 (19)	93 ± 30 (19)	85 ± 20 (17)	89 ± 24 (18)
110 ± 24 (37)	83 ± 19 (40)	74 ± 20 (37)	71 ± 17 (41)
B-113 (26) F-132 (20) F-127 (13)		96 (21) 115 (19) 117 (13)		87 (13) 92 (18) 100 (13)	83 (12) 88 (18) 94 (12)
116 ± 27 (22) 114 ± 19 (22)	98 ± 26 (22) 97 ± 16 (22)	92 ± 15 (22)
			95 ± 20 (124)
			B-91 ± 13 (39) F-95 ± 19 (141)		F-97 ± 61 (96)
121 (128)	109 (150)		88 (151)		85 (153)
128 ± 37 (8) 105 ± 20 (12)	97 ± 18 (12) 99 ± 15 (14)	91 ± 18 (17) 79 ± 12 (16)	74 ± 16 (16) 74 ± 16 (17)	62 ± 12 (15)
			76 ± 13 (19) 69 ± 12 (18) 75 ± 16 (8)	70 ± 14 (19) 67 ± 17 (18) 74 ± 16 (8)	75 ± 16 (19) 65 ± 16 (18) 71 ± 12 (8)
B-99 ± 17 (17) F-108 ± 18 (17)			74 ± 12 (15) 101 ± 9 (16)
B-101 ± 16 (10) F-118 ± 17 (10)			72 ± 9 (10) 87 ± 11 (10)
		F-104 ± 17 (40)	100 ± 10 (40)	95 ± 11 (40)	90 ± 11 (40)
			110 (29)
	102 ± 20 (60)		91 ± 18 (36)
		B-86 ± 11 (71) F-99 ± 14 (46)			80 ± 13 (56) 95 ± 15 (42)

Age (months)
7	8	9	10	11	12
		96.0 (91)
79 ± 12 (8)	74 ± 7 (7)	70 ± 14 (5)	75 ± 17 (5)	72 ± 15 (6)	77 ± 5 (2)
119 ± 41 (54)	110 ± 42 (84)	126 ± 44 (103)	120 ± 44 (92)	120 ± 40 (73)	119 ± 50 (36)
		F-99 ± 25 (32)
77 ± 16 (19) 73 ± 14 (18) 65 ± 16 (8)	72 ± 21 (18) 63 ± 18 (8)	69 ± 19 (8)
86 ± 11 (23)	82 ± 11 (7)
	108 (26)				103 (31)
		84 ± 19 (46) 94 ± 18 (41)			90 ± 18 (40) 98 ± 21 (40)

^a Abbreviations: Social economic status (SES); food composition tables (FCT); metabolizable energy (ME); gross energy (GE).

To correct test-weighing values for IWL, the number and duration of breastfeedings also must be known. The systematic bias caused by IWL may be estimated for 1-4 month-old (Butte et al 1985) and 12 month-old breast-fed infants (Dewey et al 1991). Based upon the published weights, milk intakes, number of feedings, and duration of feedings (20 min was assumed for the Dewey report), and an estimated average rate of IWL of 2 g/kg/d, IWL would cause a 4 and 6% underestimation of intake in the 1-4 month-old and 12 month-old breast-fed infants, respectively.

Figure 3 Energy intake (kcal/kg/d) of infants predicted from equation (2) - (4).

Published intakes of breast-fed infants are in terms of metabolizable energy in some reports, and gross energy in others. Gross energy intake may be converted to metabolizable energy intake using Atwater factors (Watt & Merrill, 1963). Application of the Atwater factors to human milk components (Butte et al, 1984), indicates that human milk would be 96.4% metabolizable. The applicability of the Atwater factors to infants has been questioned, since the original studies were performed on adults (Schulz & Decombaz, 1987). Balance data on ten breast-fed infants fed unpasteurized human milk are available from one study (Southgate & Barrett, 1966). Metabolizable energy averaged 92%.

If not already corrected, the energy intakes of breast fed infants presented in Table 2 were corrected uniformly for IWL and metabolizable energy. A 5% correction was applied to compensate for IWL, and metabolizable energy was assumed to be 94% of gross energy intake. The energy intakes reported by Martinez et al (1985) differed substantially from those of the other formula-fed infants. These six mean values were eliminated from the database.

All: Energy intake (kcal/kg/d)
= 121 - 10.2 age + 0.72 age²
r² = 0.43; n = 101 (2a)

BF: Energy intake (kcal/kg/d)
= 116 - 12.3 age + 0.83 age²
r² = 0.66; n = 59 (3a)

FF: Energy intake (kcal/kg/d)
= 125 - 9.3 age + 0.64 age²
r² = 0.67; n = 42 (4a)

The curvilinearity of the equation of energy intake on age has important ramifications for energy requirements during infancy. The above analysis confirms White head's earlier observations of decreasing need in the first half of infancy, followed by increasing need in the latter half of infancy. However, the above analysis may be misleading because of a mathematical artifact. Energy intake standardized by body weight was regressed on age, which was highly correlated with weight (r_{age, weight} = 0.97). By dividing the ordinate (energy intake) by the abscissa value (age) or in this case a proxy (weight) for the abscissa, a curvilinear relation is created mathematically with this quadratic equation, irrespective of the actual data (Tanner, 1949). It is misleading to describe the relationship of energy intake on age, with energy intake divided by weight.

To circumvent this artifact, another model relating energy intake (kcal/d) to age with weight as a covariate was developed. Mode refers to breast-fed (coded 0) or formula-fed (coded 1). Data were weighted for sample size.

All: Energy intake (kcal/d)
= 100 - 57.7 age + 3.3 age² + 92.8 weight + 43.6 mode + 13.8 age × mode
r² = 0.81; n = 101 (5)

BF: Energy intake (kcal/d)
= 581 - 21.7 age + 1.1 age² + 24.8 weight
r² = 0.63; n = 59 (6)

FF: Energy intake (kcal/d)
= 11.8 - 71.8 age + 4.0 age² + 130 weight
r² = 0.94; n = 42 (7)

In the regression model of all cases there was both a negative linear term (age) and a positive quadratic term (age²) (P = 0.001). A significant interaction between age and feeding mode was encountered (P = 0.006). Splitting on feeding mode, the age² terms for breast-fed and formula-fed infants were significant (P = 0.04 and 0.001, respectively). A curvilinear trend in energy intake was evident. Further analysis revealed that the curvature could be explained by a significant interaction between age and weight. Energy intake (kcal/d) can best be described by the following regression equations weighted by sample size:

All: Energy intake (kcal/d)
= 210 - 59.2 age + 37.2 mode + 63.1 weight + 14.0 age × mode + 5.6 age × weight
r² = 0.80; n = 101 (8)

BF: Energy intake (kcal/d)
= 640 + 25.6 age-40.1 weight + 1.7 age × weight
r² = 0.62; n = 59 (9)

FF: Energy intake (kcal/d)
= 101 - 89.6 age + 105 weight + 7.7 age × weight
r² = 0.87; n = 42, (10)

In the overall model, weight (P = 0.001) and the interactions of age × mode and age × weight were significant (P = 0.01 and 0.002). The older the infant the greater the positive contribution of age × weight term to energy intake becomes. Energy intake of infants across the 1st year of life is best described in this multiple regression, with weight treated as a covariate.

Energy requirements of infants have been estimated from dietary intake using equations (2a), (3a), (4a) and (8)-(10) (Table 3). NCHS median weights were used to calculate energy requirements. For the estimation of the energy requirements of all infants, it was assumed that half the infants were breast-fed and half were formula fed. The current FAO/WHO/UNU energy requirements for infants are 2-15% higher than these estimates based on energy intakes recorded after 1980. The discrepancy is partially due to the 5% increment added to the 1985 FAO/WHO/UNU energy requirements to compensate for assumed underestimation of energy intakes.

Total energy expenditure of infants

The energy requirements of older children have been estimated from multiples of basal metabolic rates (BMR), reflecting various levels of physical activity (FAO/WHO/UNU, 1985). Even though information on the BMR of infants has been available, this approach was not applicable to infants because reasonable allowances for physical activity were undefined. Newly emerging data on total energy expenditure (TEE), however, may be used to derive energy requirements of infants. TEE encompasses BMR, thermoregulation, synthetic cost of growth, and physical activity.

The doubly labeled water method for the measurement of TEE has been used and validated in a number of studies in preterm infants and hospitalized term infants. Although these validation studies were not conducted under free-living conditions of term infants, the high rates of water turnover and high percentages of body water common to all infants were tested. Mean errors between the doubly labeled water method and respiration calorimetry were 0.3 ± 2.6% (Roberts et al, 1986), - 0.9 ± 6.2% (Jones et al, 1987), - 4.5 ± 6.0% (Westerterp et al, 1991), and Ä0.4 + 11.5% (Jensen et al, 1992). Although errors for individuals may be large the doubly labeled water method provides an accurate, unbiased measurement of total energy expenditure for groups and may be used for recommendations of energy intakes of infants. Available data on the TEE of infants are summarized in Table 4. The data published by Davies et al (1989, 1991) have been updated to include more infants (Davies, 1993 private communication). There are 268 data points available on presumably well nourished infants studied in Cambridge, UK and Houston, USA. The majority (90%) of the infants studied were £ 6 months of age (specific ages given in Table 4). TEE of infants living in The Gambia (n = 59) (Prentice et al, 1988; Vasquez-Velasquez, 1987, 1988), rural Mexico (n= 38) (Butte, 1993), and Peru (n= 19) (Fjeld et al, 1989) also have been studied.

Table 3 Energy requirements of infants estimated from dietary energy intake

	Energy intake
Age (months)	All (kcal/d)	BF* (kcal/d)	FF* (kcal/d)	All (kcal/kg/d)	BF* (kcal/kg/d)	FF* (kcal/kg/d)
Boys:
0-1	453	504	470	116	110	120
1-2	490	500	520	107	99	112
2-3	530	503	573	100	90	106
3-4	571	513	625	94	83	100
4 5	612	528	675	90	77	96
5-6	650	549	721	87	73	93
6 9	730	600	812	85	70	91
9-12	863	693	963	93	78	98
Girls:
0-1	440	512	448	116	110	120
1-2	461	515	474	107	99	112
2-3	487	523	504	100	90	106
3-4	517	535	540	94	83	100
4 5	554	549	585	90	77	96
5-6	594	567	632	87	73	93
6 9	675	614	726	85	70	91
9-12	784	707	842	93	78	98

* BF Breast-fed; FF Formula-fed infants.

First, we performed an analysis on the group mean values for TEE of presumably well-nourished infants (Table 4). Mean TEE was 449 ± 161 kcal/d for infants who were 4.0 ± 3.0 months old and weighed 6.1 ± 1.5 kg. Weighted for sample size, TEE was regressed on age (months), feeding mode (breast-fed, coded 0, and formula-fed, coded 1) and weight (kg) (BMDP1R: Dixon, 1990).

TEE (kcal/d) = 73.8 + 38.6 age + 40.4 mode + 35.4 weight
SEE = 25.7
r² = 0.98;
n = 14. (11)

TEE (kcal/d) was significantly affected by age (P = 0.005), feeding mode (P = 0.01), but not weight. Weight was highly correlated with age (r = 0.98). Interactions between age, mode and weight were not significant. Mean TEE for the breast-fed and formula-fed infants were 420 ± 151 and 495 ± 190 kcal/d, respectively. The high r² does not imply that the TEE of individual infants can be predicted with such a high degree of certainty. It should be remembered that the analysis was performed on group mean values. The SEE provides an indication of the error for predicting group mean values of TEE.

Table 4 Total energy expenditure of infants by doubly-labeled water method

Reference	n	Age (months)	Fxa	RQ	TEE (kcal/d)	TEE (kcal/kg/d)	Comments
Lucas et al (1987)	12BF	0.9-1.4 2.3-2.8	0.13 0.13	0.85 0.85	306 (26)b 402 (19)	66.9 (24) 71.7 (8)	BF infants, Cambridge,UK
Roberts et al (1988)	18	3	0.13	0.87	408 (28)	72 (5)	MF infants, Cambridge, UK TEE/SMR= 1.15
Vasquez-Velasquez (1987)	8 15 19 8	0-3 3-6 6-9 9-12			381 (88) 473 (106) 572 (121) 664(133)	82 (23) 78 (21) 80 (16) 85 (12)	MF Gambian infants
Fjeld et al (1989)	22FF 19FF	16 16.3			629 (84) 692 (82)	90 (12) 84 (10)	FF infants, Lima, Peru Early recovery from malnutrition Late recovery from malnutrition
Davies et al (1989)	39c 40c 37c	1.2 2.5 6.0	0.13 0.13 0.13	0.87 0.87 0.86	306 (93) 392 (96) 605 (100)	64.5 (16.7) 66.9 (14.3) 78.9 (12.0)	BF and FF infants, Cambridge, UK
Butte et al (1990a)	10BF 10FF 10BF 10FF	1 4	0.16 0.17 0.20 0.20	0.94 0.90 0.90 0.90	291 (48) 316 (42) 420 (49) 476 (58)	64 (7) 67 (8) 64 (8) 73 (9)	BF and FF infants, Houston, TX TEE/SMR = 1.28, 1,26 TEE/SMR = 1.34, 1.36
Davies et al (1991)	33c	2.8	0.13	0.86		69 (17.9)	Same infants as 1989 paper
Davies (unpublished 1993)	20BFc 29FFc 20BFc 30FFc 19BFc 18FFc 12BF 10FF	1.4 1.4 2.8 2.8 6.0 6.0 9.2 9.2			283 (80) 319 (97) 366 (73) 433 (118) 590 (119) 619 (78) 702 (124) 808 (184)	61.1 (17.8) 71.4 (19.1) 64.5 (12.6) 75.3 (19.6) 78.5 (13.7) 79.0 (11.2) 83.0 (14.8) 93.7 (21.2)	BF and FF infants, Cambridge, UK
Davies (unpublished 1993)	24	1.4				74.5 (12.1)	BF (n = 11) and FF (n = 13) infants, Cambridge, UK
Butte et al (1993)	19BF 19BF	4 6	0.23 0.24	0.88 0.85	446 (97) 542 (83)	74.1 (13.9) 76.0 (6.9)	BF infants, Capulhuac, Mexico

^a Abbreviations: Fx = isotope fractionation; RQ = respiratory quotient; TEE = total energy expenditure; BF = breast-fed; FF = formula-fed; MF = mixed-fed; SMR = sleeping metabolic rate.
^b Mean (s.d.).
^c 1993 unpublished compilation of data used.

Standardized by body weight, TEE averaged 72.6 ± 8.1 kcal/kg/d overall, and 69.2 ± 7.8 and 76.6 ± 9.3 kcal/kg/d for the breast-fed and formula-fed infants, respectively. TEE (weighted by sample size, kcal/kg/d) was significantly affected by age (P = 0.001) and feeding mode (P = 0.01); the interaction between age and feeding mode was not significant. Within studies, the TEE of breast-fed infants has been shown to be lower than that of formula-fed infants (Butte, 1990a; Davies, 1992).

TEE (kcal/kg/d) = 60.1 + 2.6 age + 6.5 mode
SEE = 3.7
r² = 0.83; n = 14. (12)

We calculated BMR according to the Schofield equation for children under the age of 3 years (1985). Mean BMR was 54.6 ± 1.6 kcal/kg/d for the boys and 52.8 ± 1.7 kcal/kg/d for the girls. The physical activity level of the infants (TEE/BMR) increased from 1.3 at 1 month to 1.7 at 12 months of age. TEE rose steadily and gradually as activity increased through infancy.

Second, we examined the TEE data from infants living under harsh environmental conditions. We compiled 88 data points on Gambian and Mexican infants under 12 months of age (Vasquez-Velasquez, 1987; Butte, 1993). The mean TEE of these infants (5.7 ± 3.1 months) was 513 ± 101 kcal/d or 79.2 ± 4.0 kcal/kg/d. The TEE (kcal/kg/d) of infants living under harsh environmental conditions was significantly higher than that of the more sheltered infants (t = 2.6, P = 0.02), but the Gambian and Mexican infants were older. The regression of TEE (kcal/kg/d) on age did not differ between the sheltered and unsheltered infants. Prentice did not find any significant differences in TEE (kcal/kg/d) between Gambian and British infants, aged 0 to 36 months (Prentice, 1993). However, we found the TEE (kcal/kg/d) of the Mexican infants to be higher than that of predominantly breast-fed infants studied in Houston (Butte et al, 1993). More data from different geographic locations are needed to resolve putative differences in TEE of infants exposed to infection and other environmental stresses.

Currently available data on TEE of infants are limited in number, age range, and geographic distribution. Nevertheless, TEE data provide strong evidence for the need to revise current recommendations for energy intake of infants. Prudently, more data should be sought, particularly in the second 6 months of life.

Energy requirement for growth

Although the energy requirement for growth relative to maintenance is small, except for the first months of life, satisfactory growth is a sensitive indicator of whether needs are being met. To determine the energy cost of growth, the energetics of growth must be understood and satisfactory growth velocities must be defined. The 1985 requirements were based on the growth reference published for international use by WHO (1983), which were derived from the United States National Center for Health Statistics growth curves (NCHS, 1977). What constitutes appropriate infant growth is a topic of controversy and is currently under debate at WHO. Because of policy implications, the findings of the WHO Expert Committee on 'Physical Status: The Use and Interpretation of Anthropometry During Infancy' should be considered if the FAO/WHO/UNU Energy and Protein Requirements are revised. Quantitatively, revision of infant growth curves will minimally impact estimated energy requirements. If growth curves were revised to reflect the growth velocities of breast-fed infants, energy requirements would decrease by 10, 16, 24 and 12 kcal/d for 0-3 months, 3-6 months, 6-9 months and 9-12 months, respectively.

In addition to the growth velocity, the energy cost of growth must be known. This cost consists of the energy content of the newly synthesized tissues and the energy expended in synthesis. In the 1985 report the energy cost of weight gain was reviewed in Annex 4 (FAO/ WHO/UNU, 1985) The value proposed for healthy term infants was 5.6 kcal/g gained. We measured the energy cost of growth in term infants and arrived at an estimate, 4.8 kcal/g (Butte et al, 1989). An additional report appeared on the energy cost of growth of infants recovering from malnutrition; the total energy cost of growth was 6-7 kcal/g (Fjeld et al, 1989). The estimated energy cost of growth is more accurate when the separate costs of protein and fat deposition are taken into account, since the components of weight gain change dramatically through the first year of life. However, the practicality of this point is significantly diminished by the fact that the energy cost of growth as a percentage of total energy requirement decreases from 35% at 1 month to 3% at 12 months.

The total energy cost of growth and its components is presented in Table 5 (Figure 4). For the present discussion, the rates of weight gain and components of weight gain, as described by Fomon et al (1982), have been used. For lack of specific information on the composition of weight gain of breast-fed and formula-fed infants, no distinction was made with respect to potential differences in the energy cost of growth between feeding groups. Median NCHS weights were used to standardize the data. The energetic efficiencies of synthesizing protein and fat were taken to be 42% (1 kcal deposited/2.38 kcal used) and 85% (1 kcal deposited/ 1.17 kcal used), respectively (Roberts & Young, 1988). Energy equivalents for fat and protein were 9.25 kcal/g and 5.65 kcal/g, respectively.

Table 5 Energy cost of growth through infancy

			Fat deposition		Protein deposition				Total energy cost growth
Age (months)	Weight (kg)	Weight gaina (g/d)	(g/d)b	(kcal/d)c	(g/d)b	(kcal/d)c	Fat synthesis (kcal/d)d	Protein synthesis (kcal/d)d	(kcal/d)	(kcal/kg/d)
Boys:
0-1	380	29	6	56	4	21	10	29	115	30
1-2	4.75	35	14	130	4	20	23	27	201	42
2-3	5.60	30	13	119	3	17	21	23	181	32
3-4	6.35	21	8	77	2	13	14	18	121	19
4 5	7.00	17	6	51	2	11	9	16	87	12
5-6	7.55	15	4	38	2	11	7	16	72	9
6 9	8.50	13	2	17	2	11	3	16	46	5
9-12	9.70	11	1	9	2	10	2	14	35	4
Girls:
0-1	3.60	26	6	52	3	19	9	26	105	29
1-2	4.35	29	13	118	3	16	21	22	177	41
2-3	5.05	24	10	93	3	15	16	20	145	29
3-4	5.70	19	7	68	2	12	12	16	108	19
4-5	6.35	16	6	55	2	11	10	15	90	14
5-6	6.95	15	5	45	2	11	8	15	79	11
6-9	7.97	11	2	16	2	10	3	14	43	5
9-12	9.05	10	1	11	2	10	2	13	36	4

^a Monthly rates of weight gain (Fomon et al, 1982).
^b Monthly rates of &t and protein deposition (Fomon et al, 1982).
^c Energy equivalents for fat and protein deposition were taken as 9.25 kcal/g and 5.65 kcal/g, respectively.
^d Energetic efficiencies of synthesizing protein and fat were taken to be 42% (1 kcal deposited/2.38 kcal used) and 85% (1 kcal deposited/1.17 kcal used), respectively (Roberts & Young, 1988).

As calculated, the energy cost of growth displays an abrupt increase at 1-2 months, followed by a gradual decline through 12 months. The abrupt increase in fat deposition may be an artifact due to interpolation of data compiled from different studies by Fomon et al (1982). Unpublished data of Southgate were used to estimate body composition at birth. Body fat was assumed to be linearly related to subscapular and infra-iliac skinfolds between the ages of 3 months and 10 years. A smoothed curve was constructed relating the percentage body fat to age from 1 month to 10 years.

Energy requirements of infants predicted from total energy expenditure and growth

We estimated energy requirements of infants from birth to 12 months of age from total energy expenditure and energy deposition as protein and fat (Table 6, Figures 5 and 6). The energy costs of protein and fat synthesis are covered in the estimate of total energy expenditure and therefore have been excluded from this estimate of energy deposition. The relatively low energy deposition at 0-1 months and high estimate at 1-2 months may be in error. Because fat deposition probably does not increase so abruptly between 1 and 2 months, the average energy deposition for the interval 0-2 months was used in calculating energy requirements. The 1985 FAO/WHO/UNU energy requirements are 9-39% higher than these estimates. These discrepancies are not trivial and could lead to overfeeding of infants.

FIGURE 4 Energy cost of fat and protein deposition in infants (kcal/d).(Boys)

FIGURE 4 Energy cost of fat and protein deposition in infants (kcal/d).(Girls)

A comparison of FAO/WHO/UNU energy requirements and estimations based on energy intakes recorded after 1980 and on TEE and growth is graphically displayed in Figures 7 and 8.

FIGURE 5 Energy requirements of infants estimated from total energy expediture and energy deposition (kcal/d).

Recommendations

The 1985 FAO/WHO/UNU recommendations for dietary energy intake of healthy infants seem too high based on reported measurements of energy intake or energy expenditure and estimates of the energy deposited for growth. Because observed energy intakes may not reflect desirable intakes, measurements of energy expenditure are preferred as the basis for estimating energy requirements. Estimated energy requirements of infants based on total energy expenditure and growth are 9-39% lower than the 1985 FAO/WHO/UNU recommendations and provide strong evidence that current estimates should be revised. However, confirmation of this observation will require expansion of the available database on total energy expenditure of healthy infants, in terms of sample size, age range and geographic distribution across the entire age range of infancy. Data are particularly scarce in the second 6 months of infancy. Estimated energy requirements should be consistent with the growth reference endorsed by WHO. To better define the energy deposited during growth, changes in body composition during infancy must be confirmed.

Given the relative uniformity of behavior, physical activity and growth of healthy infants from different geographic origins, estimates of energy requirements can be applied universally to healthy infants. It should be appreciated that energy requirements of infants are a function of age, gender, body size and feeding mode. Stipulation of estimated energy requirements by these factors will depend on the application.

More data must be sought on the energy expenditure of infants in populations at risk of high rates of infection and exposed to other environmental sources of stress to determine if energy requirements are altered under these circumstances. The energy needs for adequate catch-up growth also must be considered.

Table 6 Energy requirement estimated from total energy expenditure and energy cost of growth

	Total energy expenditure						Energy deposition
Age (months)	ALL (kcal/d)	BFa (kcal/d)	FFa (kcal/d)	ALL (kcal/d)	BFa (kcal/d)	FFa (kcal/d)	(kcal/d)	(kcal/kg/d)
Boys
0-1	248	228	268	65	61	68	113	26
1-2	320	300	340	67	64	70	113	26
2-3	389	368	409	70	67	73	136	24
3-4	454	434	474	72	69	76	90	14
4-5	516	495	536	75	72	78	62	9
5-6	574	553	594	78	74	81	49	6
6-9	684	664	705	83	80	86	28	3
9-12	843	822	863	91	87	94	19	2
Girls:
0-1	241	220	261	65	61	68	102	22.5
1-2	306	286	326	67	64	70	102	22.5
2-3	369	349	389	70	67	73	108	20
3-4	431	411	451	72	69	76	79	13
4-5	492	472	513	75	72	78	65	10
5-6	552	532	573	78	74	81	56	8
6-9	666	645	686	83	80	86	26	3
9-12	820	799	840	91	87	94	21	2

Energy requirement
Age (months)	BFa (kcal/d)	FFa (kcal/d)	ALL (kcal/kg/d)	BFa (kcal/kg/d)	FFa (kcal/kg/d)
Boys
0-1	341	381	91	87	94
1-2	413	453	93	90	96
2-3	504	545	94	91	97
3-4	524	564	86	83	90
4-5	557	598	84	81	87
5-6	602	643	84	80	87
6-9	692	733	86	83	89
9-12	841	882	93	89	96
Girls:
0-1	322	363	88	84	90
1-2	388	428	90	86	92
2-3	457	497	90	87	93
3-4	490	530	85	82	89
4-5	537	578	85	82	88
5-6	588	629	86	82	89
6-9	671	712	86	83	89
9-12	820	861	93	89	96

^a BF = breast-fed; FF = formula-fed infants.

FIGURE 6 Energy requirements if infants estimated from total energy expenditure and energy deposition (kcal/kg/d).

FIGURE 7 FAO/WHO/UNU energy requirements compared against requirements (1) based on energy intakes observed after 1980 and (2) total energy expenditure (TEE) and energy deposition during growth (kcal/d).

FIGURE 8 FAO/WHO/UNU energy requirements compared against requirements (1) based on energy intakes observed after 1980 and (2) total energy expenditure (TEE) and energy deposition during growth (kcal/kg/d).

Acknowledgements - I wish to thank Drs PSW Davies, Cambridge, UK; KG Dewey, University of California-Davis; KF Michaelsen, The Royal Veterinary and Agricultural University, Copenhagen,
Denmark; AM Prentice, Dunn Nutrition, Cambridge, UK; AS Ryan, Ross Laboratories, Columbus, Ohio, and JE Stuff, Children's Nutrition Research Center, Houston, Texas for their contribution of data used in this manuscript, as well as Dr C Garza, Cornell University, Ithaca, New York, for his thoughtful review. I would also like to thank I Tapper for manuscript preparation, and L Loddeke and R Klein for editorial review.

This work is a publication of the USDA/ARS Children's Nutrition Research Center, Department of Pediatrics Baylor College of Medicine and Texas Children's Hospital, Houston, TX. Funding has been provided from the U.S. Department of Agriculture, Agricultural Research Service under Cooperative Agreement No. 58-6250-1-003. The contents of this publication do not necessarily reflect the views or policies of the U.S. Department of Agriculture, nor does mention of trade names, commercial products, or organizations imply endorsement by the U.S. Government.

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Discussion

Atwater factors indicate the average amount of energy yielded by one gram of ingested carbohydrate, fat or protein; they are used in the calculation of the metabolizable energy content of foods, for instance in food composition tables and in infant formulas. Atwater (as well as Durnin and Southgate after him) derived them from the heat of combustion, corrected for energy losses in the form of unabsorbed nutrients in feces and urine of adults. The question was raised whether the same factors were also applicable to infants. The answer to this question does not affect energy requirements per se but becomes important in a discussion of recommended dietary intakes. Several factors may influence the metabolizable energy derived from food: (1) the chemical form of the macronutrient in the food, (2) the coefficient of digestibility; (3) the extent to which the nutrients are not completely oxidized, but stored in the body; (4) gut maturation and (5) age. In growing infants nitrogen retention will be higher. Preterm infants absorb less fat than term infants, and fat is generally less well absorbed by newborn infants than by older infants. Fat digestibility is also highly dependent upon the fat source and its processing, e.g. butterfat is poorly absorbed, whereas a mixture of vegetable oils is absorbed nearly to the same extent as human milk. In a study of 10 breast-fed infants fed unpasteurized milk, Southgate found that metabolizable energy averaged 92%. Application of the Atwater factors to human milk components indicated 96% metabolizable energy. Using Atwater factors in normal infants, therefore, does not seem to entail great errors. Application of the Atwater factors in preterm or sick infants may overestimate energy availability.

In young infants the energy content of human milk is of particular importance. Since it is very variable throughout days and feeds and there is no generally agreed upon, standard method for obtaining representative milk samples and for estimating their energy density, published figures vary considerably. Butte et al, using different methods, obtained values between 0.65 and 0.67, whereas values from Sweden (0.72) and a WHO study in Hungary are considerably higher (Waterlow). In the first two figures of her paper, Butte used energy intakes as reported. Dewey pointed out that differences in fat secretion in breast milk between groups of women had been observed, even when exactly the same methods were used. Maternal body fat can affect milk fat (Prentice), as can fat intake in lean women (Dewey). Since pasteurization alters the fat, it is important to note whether pasteurized or non pasteurized milk is used. In the end, the prevailing opinion was that Dewey and Butte had made the most rigorous assessments and that their values should therefore be relied upon primarily.

Several participants were intrigued by the low level of the first two data points in the line representing energy requirements derived from TEE and growth in Butte's figures 7 and 8. Most likely this is an artifact due to an underestimate of the cost of growth in these first two time periods.

Should recommendations be the same or different for breast- and bottle-fed infants? Reeds argued that requirements and intakes should not be confused. Requirements are to be seen as a function of the organism and not of the diet, whereas recommended dietary allowances are a function of the diet and the degree to which it meets requirements. Dewey pointed out that in practice the picture was less clear and the feeding mode seemed to affect physiology. Energy expenditure is lower in breast-fed infants or, in other words, formula-fed infants appear to require more energy than breast-fed ones. These differences are most marked between 3 and 6 months of age; then they gradually disappear, probably as a consequence of the phasing out of pure breast-feeding. Butte tried to derive energy requirements from data of a mixed group of infants, 50% breast- and 50% formula-fed. Dewey advocated separate recommendations for the two feeding groups in order to avoid the :impression that breast-fed infants do not get enough energy and ought to be supplemented or the risk that formula fed infants will not get enough energy to cover their needs. Giving a wide range of requirements does not appear to be a satisfactory solution either.

Butte et al tried to determine how much of a difference in diet-induced thermogenesis (DIT) there was between breast- and formula-fed infants. During the first 4h after the meal, DIT appeared slightly lower in breast-fed infants, but the difference was not statistically significant.

Waterlow queried the validity of 42% for the energetic efficiency of protein synthesis (Table 5, footnote d), and suggested that a figure of 75% would be more in accordance with the evidence.

Do infants growing up in the more stressful environment of developing countries or urban slums have the same or higher energy requirements than infants in industrialized countries? The little information that exists on this issue shows smaller differences than expected. Total energy expenditure (TEE), expressed as kcal/kg, was for instance very similar in infants from The Gambia and the UK (Prentice). Butte compared TEE of small groups (n = 20) of 4-month-old infants from Mexico and Houston. In. Mexico it was 74 kcal/kg, in Houston 64 and 73 kcal/kg for breast- and bottle-fed infants, respectively. Several participants felt that more information was needed to decide the extent to which frequent infections and desirable catch-up growth add to energy requirements in poor environments.