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close this bookEnergy and Protein requirements, Proceedings of an IDECG workshop, November 1994, London, UK, Supplement of the European Journal of Clinical Nutrition (International Dietary Energy Consultative Group - IDECG, 1994, 198 pages)
close this folderEnergy requirements of pregnant and lactating women
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View the documentIntroduction
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(introductory text...)

AM Prentice1, CJK Spaaij2, GR Goldberg1, SD Poppitt1, JMA van Raaij2, M Totton1, D Swann1 and
AE Black1

1 MRC Dunn Clinical Nutrition Centre, Hills Road, Cambridge CB2 2DH; 2 Department of Human Nutrition
Agricultural University of Wageningen, The Netherlands

Descriptors: pregnancy, lactation, energy requirements

Introduction

The 1985 FAO/WHO/UNU recommendations for energy and protein requirements were based on a meeting of an expert panel held in October 1981 as the culmination of a review process initiated soon after the publication of the 1973 guidelines (FAO/WHO/UNU, 1985). Since this time a considerable amount of new data have been collected in the fields of pregnancy and lactation. Much of the research, particularly with respect to pregnancy, has been specifically directed towards the definition of recommended dietary allowances and therefore permits a thorough review of the 1985 recommendations.

In this position paper we review the new data in some detail, and attempt to resolve outstanding areas of controversy especially those relating to the apparent mismatch between estimated incremental needs and observed energy intakes. We explore alternative methods for expressing the incremental requirements for reproduction to bring them closer into line with the use of physical activity levels (PALs) as applied to other adults.

The existing FAO/WHO/UNU recommendations for pregnancy and lactation are summarised in Tables 1 and 2 and compared with some other recent guidelines from affluent nations.

Pregnancy

The 1985 values were based on a general acceptance of Hytten's estimate that the total energy needs of pregnancy amount to 335 MJ (80000 kcal) or about 1.2 MJ/ day (285 kcal/day; Hytten & Chamberlain, 1980). There was a clear recognition that this rather small increment could be greatly influenced by possible changes in physical activity, and that a reduction in activity might explain why 'many recent studies of food intakes of well nourished pregnant women indicate that the extra energy requirements for tissue deposition are not always accompanied by commensurate increases in intake'. The recommended increment of 1.2 MJ/day was applied evenly across pregnancy because 'some fat should be deposited early in pregnancy, and because appetite and periodic work requirements vary greatly'. It was considered reasonable to reduce the average additional allowance to 0.84 MJ/day (200 kcal/day) where healthy women reduce their activity. Table 1 highlights the wide differences in allowances between various reports. These reflect both differences in interpretation of the available data and in underlying philosophy. Most reports published after 1985 have recommended lower increments than the FAO/WHO/UNU figure.

Correspondence: AM Prentice.

Lactation

The 1985 recommendations were based on the median milk consumption of breast-fed Swedish infants for the first 6 months and on more limited data from a number of populations for later periods. It was assumed that milk energy was 2.9 kJ/g (0.7 kcal/g) and the efficiency of conversion of dietary to milk energy was 80%. Furthermore it was assumed that the average woman would start lactation with 150 MJ (36000 kcal) of additional fat reserves (laid down in pregnancy) and that these would be used to subsidise the cost of lactation over the first 6 months thus yielding about 0.84 MJ/day (200 kcal/day). It was stated that allowances 'will need to be adjusted according to maternal fat stores and patterns of activity', but no additional figures were provided.

It can be seen from Table 2 that there is a much greater international consensus regarding recommended allowances for lactation than for pregnancy (Table 1) There has not been such a pronounced trend towards lowering allowances for lactation as there has been for pregnancy.

Recent advances in understanding the links between maternal nutrition and the well-being of her offspring

Since 1985 there have been major advances in our understanding of the potential influence that a mother's nutrition can have on the health of her children. In particular, the work of Barker (1992) and his colleagues on the fetal origins of adult disease has demonstrated that the pattern of fetal growth is a strong predictor of later susceptibility to diseases of affluence such as cardiovascular disease, non-insulin dependent diabetes, hypertension and hyperlipidaemia (Goldberg & Prentice, 1994). These findings re-emphasise the importance of ensuring optimal maternal nutrition, and indicate an urgent need to revise the previous assumption that a pregnancy had been successful if it resulted in a baby of viable birthweight. In our opinion such findings point to a need to err on the side of plenty when setting allowances.

Table 1 Existing FAO/WHO/UNU recommendations for pregnancy and comparison with UK, USA and Dutch values

Recommendations

Stages of pregnancy

Increment (MJ/day)

Total for pregnancy (MJ)

Qualifying comments

FAO WHO/UNU

All

1.20

336



All

0.84

235

For healthy women who reduce activity

UK

Last trimester

0.80

74

Underweight women and those not reducing activity may need more

USA

Last two trimesters

1.25

233


The Netherlands

All

0.60

168

Reduction in physical activity is assumed

From FAO/WHO/UNU (1985), COMA (1991), NAS (1989), Dutch Expert Committee (1981).

Table 2 Existing FAO/WHO/UNU recommendations for lactation and comparison with UK, USA and Dutch values

Recommendations

Stage of lactation (months)

Increment (MJ/day)

Qualifying comments

FAO/WHO/UNU

Up to 6

2.93

No fat utilisation assumed


Up to 6

2.10

Assumes fat utilisation of approx. 500 g month


After 6

2.10


UK

0-1

1.90



1-2

2.20

Assuming fat utilisation of approx. 500g/month


2-3

2.40



3-6

2.00

Rapid weaners


After 6

1.00



3-6

2.40

Slow weaners


After 6

2.30


USA

Up to 6

2.10

Assumes fat utilisation of 300-500 g/month


Up to 6

2.70

Following suboptimal pregnancy weight gain or for low maternal W/H

The Netherlands

Up to 6

2.50

Assumes fat utilisation of approx. 350g/month

From FAO/WHO/UNU (1985), COMA (1991), NAS (1989), Dutch Expert Committee (1981).

Psychological impact of setting 'minimalist' allowances for pregnancy

The trend towards reduced allowances in pregnancy has been fuelled by the desire to ensure that recommended allowances are not at variance with observations of increased food intake. The apparent paradox between estimates of needs and estimates of intake has been explained away by assuming that physical activity naturally decreases in pregnancy or that women are capable of energy-sparing alterations in metabolism. We recommend that such arguments are introduced only with great caution since women in developing countries may be prevented from reducing their activity by the constraints of a subsistence livelihood. Furthermore it must be made quite clear that, although energy-sparing metabolic adjustments may help women to carry a pregnancy to term under harsh nutritional conditions, such adjustments almost certainly result in health costs to both the mother and the baby. They should never be equated with optimal performance. To this end we recommend that allowances should clearly reflect the full costs of pregnancy and lactation, and that conditional reductions should receive less prominence than in the past.

Pregnancy

Energy cost of pregnancy: increased tissue mass

Weight gain during pregnancy comprises the products of conception (fetus, placenta, amniotic fluid), and hypertrophy of several maternal tissues (uterus, breasts, blood, fat stores, extracellular extravascular fluid). An extensive review of the associated energy costs has been presented by Hytten (1991) and is summarised in Table 3. Protein is laid down predominantly in the fetus (44%), but also in the uterus (17%), blood (14%), placenta (10%) and breasts (8%). In contrast, fat deposition takes place predominantly in maternal adipose tissue (85%), with the fetus the only other major site of importance (14%). The gain in fat stores is by far the largest component of the energy cost of tissue deposition (72%). The fetus accounts for 19% and the placenta, uterus, blood volume and breasts 2%, 3%, 3% and 2%, respectively.

Hytten's review did not include a substantial number of relatively new longitudinal studies of changes in fat mass during pregnancy in which estimates of total fat gain, or the gain in maternal fat stores, represented 83% and 72% respectively of the energy costs associated with weight gain. Those new longitudinal studies which include both baseline values before pregnancy or in the first 12 weeks of gestation and values near term or during the first two months post partum are reviewed below. The 'whole-body' measurements of total body water (TBW, from isotope dilution) or estimates of body density (BD, from underwater weighing), were considered to give the best estimates of fat mass in late pregnancy. For estimates of fat gain derived from the sum of four skinfold thicknesses, post-partum rather than late-pregnancy values were used, because changes other than fat accumulation might influence skinfold thicknesses in late pregnancy.

Fat gain during pregnancy in developed countries. The results of 15 longitudinal studies are summarised in Table 4. The average gain in fat mass by late pregnancy estimated from TBW was 3.3 kg (Forsum et al, 1988; Goldberg et al, 1993; Hytten et al, 1966; Pipe et al, 1979; Taggart et al, 1967). In the two studies which measured BD the average increase in fat mass was 2.44 kg (Spaaij, 1993; van Raaij et al, 1988). Fat gain estimated from skinfolds was substantially lower and averaged only 1.2 kg. Part of this difference is attributable to the timing of the second measurement: TBW and BD measurements were made in late pregnancy, whereas the skinfold measurements were made post partum after the fat that was not deposited in maternal stores had been lost. The fat gains estimated from TBW and BD measurements need to be reduced by about 0.4 kg (representing the fat in the fetus), in order to estimate fat deposited in maternal stores (Table 3). The fat deposition estimated from TBW measurements is then 2.9 kg, and from BD 2.0 kg. The average gain in fat stores estimated from skinfolds (1.2 kg) is thus still substantially lower. Several authors have shown that some skinfolds increase more than others during pregnancy, indicating that fat deposition is not equally distributed over all adipose tissue sites. This applies particularly to the gluteal and upper thigh regions which are not included in the traditional four site measurements. As a consequence, the validity of fat gain estimated with the skinfold technique is questionable.

Table 3 Site-specific protein and fat deposition during pregnancy, and energy costs involveda in a reference woman with a pregnancy weight gain of 12.4 kg delivering a baby of 3.3 kgb


Weight gain (g)

Energy cost (kJ)b

Site

Protein

Fat

Water

Total

Protein

Fat

Total

Fetus

440

440

2414

3294

12760

20240

33000

Placenta

100

4

540

644

2900

184

3084

Amniotic fluid

3

0

792

795

87

0

87

Uterusc

166

4

800

970

4814

184

4998

Breasts

81

12

304

397

2349

552

2901

Blood

135

20

1287

1442

3915

920

4835

Waterd

0

0

1496

1496

0

0

0

Subtotal

925

480

7633

9038

26825

22080

48905

Fat storese

67

2676

602

3345

1943

123096

125039

Total

992

3156

8235

12383

28768

145176

173944

a The energy needed for synthesis and deposition was assumed to be 29 kJ/g for protein and 46 kJ/g for fat (Durnin 1987). We later reduce the assumption for fat to 39 kJ/g.
b Values obtained from Hytten (1991).
c Blood-free uterus.
d Extracellular extravascular water, assuming that there is no generalised edema.
e The only adaptation we made to Hytten's value, was in the amount of fat laid down in maternal fat stores. The gain in adipose tissue is the difference between body weight gain and the sum of weight gains of fetus, placenta, amniotic fluid, uterus, breasts, blood and extracellular extravascular fluid. Hytten assumed this gain to be 100% fat, whereas in the table, the gain in adipose tissue is assumed to consist of 80% fat, 18% water and 2% protein (Garrow, 1978)

We also accept that the two whole-body methods give the best estimate of fat gain during pregnancy. Combining the methods results in an average total fat gain of 3.0 kg by late pregnancy and a gain in maternal fat stores of 2.6 kg. Note that this is very similar to Hytten's (modified) estimate (Table 3). The gain in maternal fat stores estimated by factorial analysis of weight gain was 3.0 kg (Table 4).

Fat gain during pregnancy in developing countries. In the only study from a developing country (The Gambia), in which TBW was measured, average fat gain was only 0.9 kg (Lawrence et al, 1987a), and the gain in maternal stores was estimated to be 0.4 kg.

Other studies from developing countries have used the skinfold technique (Barba, 1995; Thongprasert et al, 1987; Tuazon et al. 1987) and the average fat gain observed was 1.47 kg. The data are subject to the same drawbacks outlined above. The gain in maternal fat stores estimated by factorial analysis of weight gain was 1.3 kg.

In summary we recommend continued use of Hytten's estimates of the energy deposited as new tissue as set out in Table 3, but with a reduction in the assumption for maternal fat. The costs of deposition can be presented as 30 MJ (7200 kcal) for the fetus and 112 MJ (26 700 kcal) for the mother, or as 29 MJ (6900 kcal) for protein and 113 MJ (27000 kcal) for fat (mother and fetus combined).

Assuming a desirable fat gain of 2.5 kg in the maternal compartment and 0.4 kg in the fetus represents a reduction of about 0.5 kg from the 1985 value. Assuming the cost of deposition to be 39 kJ/g (9.3 kcal/ g), the total costs of fat gain are therefore 98 MJ (24 400 kcal) for the mother and 16 MJ (3800 kcal) for the fetus. Energy deposition can be assumed to be 0.4, 0.7 and 0.5 MJ/day (95, 165 and 120 kcal/day) in the three trimesters.

Energy cost of pregnancy: change in basal metabolic rate As a result of the increased tissue mass, maintenance costs rise during pregnancy, and this increase in basal metabolic rate is one of the :major components of the energy costs of gestation. In this section, an overview is given of changes in basal or resting metabolic rate (BMR or RMR) measured in recent longitudinal studies conducted in various countries.

Description of studies reviewed. During the past 10 years, nine prospective, longitudinal studies have been published which included measurements of changes in BMR throughout pregnancy. Five studies were performed in affluent, developed countries namely Scotland (Durnin et al, 1987), England (Goldberg et al, 1993), Sweden (Forsum et al, 198,3) and The Netherlands (Spaaij, 1993; van Raaij et al, 1987). The remaining studies were conducted in the poorer, less developed countries of Thailand (Thongprasert et al, 1987), The Philippines (Tuazon et al, 1987) and The Gambia (Lawrence et al, 1987b; Poppitt et al, 1993). Data in the Gambian study conducted by Lawrence were collected from two separate groups, one of which was provided with a high energy supplement throughout pregnancy.

Table 4 Longitudinal estimates of fat gain in pregnancy



Measurement periods

Weight gain




Reference

n

Baseline

Near term

Observed (kg)

Extrapolateda (kg)

Birthweight (kg)

Fat gainb (kg)

Gain in adipose tissuee (kg)

Total body water:

Hytten et al (1966)

75

10 weeks pregnant

38 weeks pregnant

11.15

12.6

3.47

2.65

3.38

Taggart et al (1967)

48

10 weeks pregnant

38 weeks pregnant

11.00

12.4

3.38

3.00

3.27

Pipe et al (1979)

27

11 weeks pregnant

37 weeks pregnant

10.40

12.6

3.45

2.50

3.40

Lawrence et al (1987)d

21

Pre- or early-pregnant

36 weeks pregnant

6.25

7.2

2.96

- 0.30

- 1.37


29

Pre- or early-pregnant

36 weeks pregnant

8.00

9.2

2.99

2.00

0.62

Forsum et al (1988)

22

Pre-pregnant

36 weeks pregnant

11.70

13.4

3.56

5.40

4.14

Goldberg et al (1993)

12

Pre-pregnant

36 weeks pregnant

11.91

13.7

3.77

2.77

4.18

Under-water weight:

van Raaij et al (1988)

42

11 weeks pregnant

35 weeks pregnant

9.15

12.0

3.46

2.50

2.74

Spaaij (1993)

26

Pre-pregnant

35 weeks pregnant

11.71

13.7

3.52

2.37

4.63

Skinfold thickness:

Pipe et al (1979)

27

12 weeks pregnant

10 weeks post partum

Ä0.1

12.9

3.45

- 0.2

- 0.6

Durnin et al (1987)

88

10 weeks pregnant

5 weeks post partum

3.1

12.4

3.37

1.7

2.7

van Raaij et al (1987)

57

Pre-pregnant

4 weeks post partum

2.9

11.6

3.46

1.9

2.5

Thongprasert et al (1987)d

25

10 weeks pregnant

4 weeks post partum

2.4

9.6

2.98

1.1

2.0

Tuazon et al (1987)d

40

13 weeks pregnant

6 weeks post partum

2.4

10.3

2.89

1.3

2.0

Spaaij (1993)

26

Pre-pregnant

4 weeks post partum

2.9

13.7

3.52

1.3

2.5

Barba et al (in preparation)d

40

Pre-pregnant

6 weeks post partum

3.5

9.4

2.85

0.9

3.1

a Body weight gain was extrapolated to the full 40 week period, assuming that the average weight gain during the first 10 weeks of pregnancy is 0.65 kg, and that body weight increases by 0.40 kg/week towards term (Hytten, 1991).
b Estimated, from actual measurements.
c Gain in adipose tissue was calculated by factorial analysis: subtracting birthweight (and placental weight), as well as Hytten's estimate for the increased weights of placenta, uterus, breasts, blood, extracellular extravascular and amniotic fluids (5.75 kg, or, excluding placental weight, 5.1 kg) from pregnancy weight gain.
d Developing country.

All the studies reported changes in BMR during pregnancy relative to either a pre-pregnancy or an early pregnancy (10-18 weeks) baseline (Table 5). Measurements were made under standardised conditions (rest, post-absorption and thermoneutrality), and gaseous exchange was measured using a Douglas bag, ventilated hood or whole-body indirect calorimeter. The costs of maintaining the fetus and other products of conception were calculated as the cumulative change in BMR throughout pregnancy measured up to 35/36 weeks (Durnin et al, 1987; Lawrence et al, 1987a; Spaaij, 1993; Thongprasert et al, 1987; van Raaij et al, 1987) or up to 40 weeks or term (Forsum et al, 1988; Goldberg et al, 1993; Poppitt et al, 1993; Tuazon et al, 1987).

Variability of changes in BMR between populations. Figure 1 shows the mean changes in BMR measured longitudinally every 6 weeks. The data have been separated into two groups representing developed (left hand panel) and less developed (right-hand panel) countries. There is a clear divergence between the women from affluent and developing countries. In the former, BMR increased rapidly in response to pregnancy. In the latter the increase in BMR was delayed and, in the Gambian women, was preceded by a rapid fall early in gestation. The most striking feature of Table 5 is the wide variability in cumulative maintenance costs among populations. These costs range from an average of +210 MJ (+50 200 kcal) in the Swedish women to - 45 MJ ( - 10 750 kcal) in unsupplemented Gambian women. For the purpose of formulating energy requirements of pregnancy, changes observed in healthy populations with favourable pregnancy outcome should be the criteria. The average is 159 MJ (38000 kcal), which is remarkably close to the original estimate of 150 MJ based on literature values of changes in oxygen consumption of individual organs and processes (Hytten & Chamberlain, 1980). Average increases over the first, second and third trimester of pregnancy were +0.2, + 0.4 and + 1.1 MJ/day ( + 48, + 96 and + 263 kcal/ day), respectively; average percentage increases above non-pregnant non-lactating (NPNL) BMR were +4%, + 7% and + 19%.

Variability of changes in BMR within populations (between subjects). Only three studies give information on the between-subject variability in maintenance costs. In Figure 2 the cumulative changes in BMR of women from England (Goldberg et al, 1993), The Netherlands (Spaaij, 1993) and The Gambia (Poppitt et al, 1993) illustrate a wide range between individuals in each population. Since the cumulative increase in BMR during pregnancy constitutes a large proportion of the total energy costs, this variability will have an important influence on extra daily requirements for individuals. Although this substantial between-subject variability has no impact on the formulation of recommended daily intakes (which are expressed for population groups), it emphasises the difficulty of making any prescriptive recommendations for individuals.

Determinants of changes in BMR. To identify the nutritional factors which influence pregnancy maintenance costs, a regression analysis on the mean values from the nine studies was performed. Correlations were calculated between the cumulative maintenance costs and each of the following variables: pre-pregnancy height, pre-pregnancy weight, pre-pregnancy fat-free mass, pre-pregnancy fat mass, pre-pregnancy percentage fat, weight gain during pregnancy, fat gain during pregnancy, and birthweight. The maintenance costs were most strongly correlated with the fatness of the women before they became pregnant (r = + 0.72, p < 0.001) and the amount of weight gained during pregnancy (r = +0.79, p < 0.001, Figure 3). These two variables were themselves highly correlated (r= +0.88, p < 0.001). From the regression line in Figure 3, it appears that for a favourable weight gain during pregnancy (approx 12.5 kg), the cumulative increase in BMR is about 160 MJ (38 000 kcal).


Figure 1
Mean changes in BMR measured longitudinally throughout pregnancy. Left-hand panel, developed countries: Scotland: triangles (Durnin et al, 1987); The Netherlands: open circles (van Raaij et al, 1987); Sweden: closed circles (Forsum et al. 1988); England: closed squares (Goldberg et al, 1993); The Netherlands: open squares (Spaaij, 1993). Right-hand panel, developing countries: The Gambia-supplemented: open squares, The Gambia-unsupplemented: closed squares (Lawrence et al, 1987); Thailand: triangles (Thongprasert et al, 1987); The Philippines: open circles (Tuazon et al, 1987); The Gambia: closed circles (Poppitt et al, 1993).

There is evidence from English (Goldberg et al, 1993) and Dutch studies (Spaaij, 1993) that the highly individual metabolic response to pregnancy may also be directed by pre-pregnancy fatness on an individual basis. However, three tertiles of Scottish women, grouped according to their initial percentage body fat, did not show different changes in BMR during pregnancy (Durnin, 1992). Unfortunately, no correlation coefficients between initial fatness and changes in BMR were given. Poppitt et al, (1993) also found no relationship between pre-pregnancy body fatness and cumulative maintenance costs. However, the range of pre-pregnancy fatness in the marginally nourished Gambian women was narrow.

The associations between maintenance needs, pregnancy weight gain and pre-pregnancy fatness are important in the development of energy recommendations. They indicate that achieving a target weight gain (approx 12.5 kg) will necessarily be associated with high maintenance costs (approx 160 MJ). They also indicate that many populations may be found to have lower maintenance requirements, but that these will probably be associated with inadequate weight gain and should not therefore be used for the formulation of energy recommendations.

Prediction of BMR during pregnancy. In non-pregnant women, BMR (MJ/day) can be predicted from body weight (kg), height (m) and age (y) with the Schofield equations (Schofield et al, 1985) which were used in the 1985 WHO/FAO/UNU report. No predictive equations are available for different stages of gestation. We compared three methods to predict BMR during pregnancy. In method 1 the Schofield equations were applied to data from pregnant women, using their body weight in pregnancy. In method 2 the equations were used to predict non-pregnant BMR from pre-pregnancy body weight. This estimate was then corrected by adding a factor specific for each trimester ( + 0.2, + 0.4 and + 1.1 MJ/day for the first, second and third trimesters, respectively). In method 3 the same estimates of pre-pregnancy BMR were corrected using a multiplication factor (1.04, 1.07 and 1.19 for the first, second and third trimesters, respectively). The three methods were compared using data from individual women from England (Goldberg et al, 1993) and The Gambia (Poppitt et al, 1993). Method 2 provided the best prediction. We therefore recommend that, if the BMR × PAL system is to be used for pregnancy, BMR should be calculated by adding increments of 0.2, 0.4 and 1.1 MJ in the three trimesters to NPNL BMR predicted from the Schofield equations.

Table 5 Population characteristics

Country:
n:

Scotland 88

England
12

Sweden 22

Netherlands I 57

Netherlands II 26

Thailand 44

Philippines 40

Gambia IS 29

Gambia IU 21

Gambia II 21

Methodology

Douglas bag

Whole-body calorimetry

Douglas bag

Douglas
bag

Ventilated hood

Douglas bag

Douglas bag

Douglas bag

Douglas bag

Ventilated hood

Age (y)

28

29

29

29

29

23

24

25

27

28

Parity

1.0

1.1

1.2

1.1

-

1.7

2.6

3.7

4.0

5.2

PP heighta (m)

1.62

1.64

1.65

1.69

1.69

1.52

1.51

1.57

1.58

1.57

PP weight (kg)

57.3

61.7

61.0

62.5

62.6

47.6

44.5

51.2

51.6

52.0

PP BMI (kg m2)

21.8

22.9

22.3

21.9

21.9

20.6

19.5

20.8

20.7

21.2

Baselinea (n)

PP = 20

PP = 12

PP = 22

PP = 23

PP = 26

EP = 44

EP = 40

PP = 40

PP = 21



EP = 68


EP = 34



EP = 12





Cumulative maintenance
(MJ)

126

124

210

144

189

100

89

4

- 45

27

S Supplemented with energy-dense groundnut biscuits.
U Unsupplemented.
a PP = pre-pregnant; EP = early pregnancy.

Energy cost of pregnancy: change in diet-induced thermogenesis

Diet-induced thermogenesis (DIT) is the energy used for the digestion, absorption, transport, and metabolism of food, and the deposition of nutrients. In the non pregnant state, DIT is equivalent to about 10% of energy intake and a reduction in this component of energy expenditure could be one of the mechanisms by which women might save energy to meet the increased energy demands of pregnancy.


Figure 2
The cumulative change in BMR of individual women from England (Goldberg et al, 1993), The Netherlands (Spaaij, 1993) and The Gambia (Poppitt et al, 1993).


Figure 3
Regression correlations between pre-pregnancy % fatness (top) and pregnancy weight gain (bottom) and the cumulative change in BMR during pregnancy. References as Figure 1.

Two longitudinal studies have been published on changes in DIT in response to a standardised liquid meal during pregnancy. In one (Illingworth et al, 1987) a significantly lower effect ( - 28%) was observed in the second trimester compared to post partum, but not in the first and third trimesters ( - 1% and Ä15%, respectively). There are however a number of methodological problems with this study. In the other study (Spaaij et al, 1994b) DIT was virtually unchanged during pregnancy compared to pre-pregnancy baseline measurements. Changes relative to the pre-pregnancy value were - 1%, - 5% and -5% in weeks 13, 24 and 35 of gestation, respectively.

Prentice et al (1987, 1989) derived the energy costs of DIT plus minor physical movements from 24h energy expenditure measurements in a whole-body calorimeter. Over all measurement periods, the within-subject coefficient of variation was only 6%, equivalent to 0.8% of total expenditure, indicating that any changes in thermogenesis were biologically insignificant.. Schutz et al (1988) also determined longitudinal changes in DIT from respiration chamber measurements. Expressed as a percentage of energy intake, DIT was significantly lower during pregnancy (9 ± 1%) than NPNL (13.5 ± 1%).

Two cross-sectional studies of DIT have been published in which pregnant and non-pregnant women were compared. They show conflicting results. Nagy & King (1984) found no significant differences between six early-pregnant, four late-pregnant and six non-pregnant women, whereas Contaldo et al (1987) found DIT to be significantly lower ( - 35%) in five late-pregnant compared to five non-pregnant women. However, as a result of the large variability in DIT, the statistical power of such small cross-sectional studies is low.

We conclude that it is reasonable to assume that DIT remains essentially unaltered during pregnancy when expressed as a proportion of energy intake.

Energy cost of pregnancy: change in energy cost of activity

During pregnancy the energy cost of a given activity might increase as a result of body weight gain, especially if the activity involves movement of the whole body. The amount of energy expended under free-living conditions might also alter as a result of behavioural changes with respect to the type of activity, and in the pace or intensity at which it is carried out. We have reviewed the studies in which changes in the energy cost of non-weight-bearing (cycle ergometer exercise) and weight-bearing (treadmill exercise and step-test) activities were measured under laboratory conditions at a standard pace and/or intensity. Only studies which provided data on basal, resting or sleeping metabolic rates were included, so that the net cost of activity (gross energy cost minus BMR) and physical activity ratios (PAR, energy cost divided by BMR) could be determined.

Energy cost of standardised non-weight-bearing activity. Changes in the energy cost of cycle ergometer exercise are presented in Figure 4. All studies were carried out in developed countries and all except two (Blackburn & Calloway, 1976; Seitchik, 1967) described longitudinal changes during pregnancy. The left-hand panel shows the changes in gross energy expenditure. Up to 35 weeks gestation, cycling metabolic rate (CMR) changed little compared to the baseline value (average 16.7kJ/ min or 4.0 kcal/min), and during the final 5 weeks most studies showed an increase (average + 1.9 kJ/min, +0.5 kcal/min or + 11.4%). The net cost of cycling was on average slightly below the non-pregnancy level up to 35 weeks (Figure 4, central panel) and only increased slightly above the non-pregnancy baseline from 35 to 40 weeks gestation, ( + 0.8 kJ/min, + 0.2 kcal/min or + 6%). The PAR progressively and almost linearly decreased during pregnancy (Figure 4, right-hand panel). The initial value averaged 4.0 and at the end of pregnancy had decreased by about 0.6 points or 15%. It appears that the change in CMR during pregnancy is not proportional to the change in BMR.

We conclude that the net cost of non-weight-bearing activity can be assumed to change little until very late in pregnancy when it increases by about 10%. The gross cost therefore tends to increase in line with changes in BMR. The PAR decreases in late pregnancy because the denominator (BMR) rises.

Energy cost of standardised weight-bearing activity. In Figure 5 the results of the six treadmill studies are summarised. Three were conducted in developed countries (Blackburn & Calloway, 1985; Durnin, 1991; van Raaij et al, 1990b) and three in developing countries (Heini et al, 1992; Poppitt et al, 1993; Thongprasert & Valyasevi, 1986). All studies except one (Heini et al, 1992) were longitudinal.

In developed countries despite the weight gained during pregnancy, the gross energy expended during treadmill walking (TMR, Figure 5 left-hand panel) was unchanged up to about 25 weeks gestation. Thereafter an increase was observed (average + 2.7 kJ/min, +0.6 kcal/min or +19%). The change in the net costs (Figure 5 central panel) was similar to that of the gross costs. The PAR was slightly reduced throughout gestation (Figure 5 right-hand panel) and by the end of pregnancy averaged 0.33 points (8.7%) below the baseline value.

In developing countries (Figure 5 left-hand panel) there was a much smaller increase in gross TMR by the end of pregnancy (0.6 kJ/min, 0.15 kcal/min or 7%). As observed in the developed countries, the results differed substantially averaging -0.7, + 1.0 and + 1.5 kJ/min ( 0.17, +0.25, +0.36 kcal/min or -8.4%, + 10.5% and +17.4%) in the studies by Poppitt et al (1993), Thongprasert et al (1987) and Heini et al (1992), respectively. There was virtually no change in the net costs (Figure 5 central panel). Near term, the average change relative to the baseline value was -0.4 kJ/min ( - 0.10 kcal/min) or -9.6% in the two longitudinal studies (Poppitt et al, 1993; Thongprasert et al, 1987). The PAR was slightly reduced during gestation (Figure 5 right-hand panel) and at the end of pregnancy averaged 0.32 points below the baseline value ( - 13.1%).


Figure 4
Changes in the energy cost of cycle ergometry exercise during pregnancy. Mean indicated by dashed line. Data from Uleland et al (1973), Blackburn et al (1974); Pernoll et al (1975); Blackburn et al (1976); Edwards et al (1981); de Groot et al (1994); Prentice et al (1989); Blackburn et al (1985); Seitchik et al (1967); Spaaij (1993). Change in CMR (kJ/min)


Figure 4 Changes in the energy cost of cycle ergometry exercise during pregnancy. Mean indicated by dashed line. Data from Uleland et al (1973), Blackburn et al (1974); Pernoll et al (1975); Blackburn et al (1976); Edwards et al (1981); de Groot et al (1994); Prentice et al (1989); Blackburn et al (1985); Seitchik et al (1967); Spaaij (1993). Change in CMR-BMR (kJ/min)


Figure 4
Changes in the energy cost of cycle ergometry exercise during pregnancy. Mean indicated by dashed line. Data from Uleland et al (1973), Blackburn et al (1974); Pernoll et al (1975); Blackburn et al (1976); Edwards et al (1981); de Groot et al (1994); Prentice et al (1989); Blackburn et al (1985); Seitchik et al (1967); Spaaij (1993). Change in PAR (kJ/min)


Figure 5
Changes in the cost of treadmill exercise during pregnancy. Developed countries: closed circles. Mean of studies from developed countries indicated by dashed line. Data from van Raaij et al (1990); Durnin (1991); Thongprasert & Valyasevi (1986); Heini et al (1992); Poppitt et al (1993); Blackburn et al (1985). Change in TMR (kJ/min)


Figure 5 Changes in the cost of treadmill exercise during pregnancy. Developed countries: closed circles. Mean of studies from developed countries indicated by dashed line. Data from van Raaij et al (1990); Durnin (1991); Thongprasert & Valyasevi (1986); Heini et al (1992); Poppitt et al (1993); Blackburn et al (1985). Change in TMR-BMR (kJ/min)


Figure 5 Changes in the cost of treadmill exercise during pregnancy. Developed countries: closed circles. Mean of studies from developed countries indicated by dashed line. Data from van Raaij et al (1990); Durnin (1991); Thongprasert & Valyasevi (1986); Heini et al (1992); Poppitt et al (1993); Blackburn et al (1985). Change in PAR

Prentice et al (1989) measured changes in the energy cost of another weight-bearing exercise: stepping on the spot up and down from a block (step test). The changes observed were similar to the average changes in the treadmill studies from developed countries.

We conclude that the net cost of walking stays fairly constant during the first half of pregnancy and then increases progressively to about 15% above the non pregnancy cost. The gross cost, which incorporates changes in BMR, increases by about 20% by term. As for non-weight-bearing exercise the PAR decreases due to the change in BMR.

One general comment should be made about expressing the cost of an activity as a PAR during pregnancy. PAR values describe the 'heaviness' of an activity and enable the intensity of different activities to be compared. This is so not only for NPNL, but also for pregnant women. However, the data presented above show that, when the intensity of an activity is kept constant, PARs decrease throughout pregnancy. This reduction at a fixed work output shows that PARs for non pregnant women should not be applied to pregnant women without modification.

Energy cost of self-paced activity. Two studies have examined changes in the energy expended on self-paced walking during pregnancy. In one study (van Raaij et al, 1990b) the measurements were made on a treadmill and walking pace was adjusted to the subjects' convenience. In the other study (Nagy & King, 1983) subjects carried a Douglas-bag on a back-pack frame when walking around a 400 m track. The pattern of changes observed in these two studies was totally different. van Raaij et al, observed a decrease in the net cost of self-paced walking (average -12%), and Nagy & King found an increase (average + 8%). Walking pace decreased by 4% and 12%, respectively.

We conclude that the net cost of self-paced walking increases during pregnancy if behavioural changes are limited, which is in line with the (more pronounced) increase of the net cost of fixed-pace walking. However, if women substantially reduce their walking pace during pregnancy, the net cost of the activity might decrease.

Changes in activity patterns (time-motion studies). In time-motion studies, the type and duration are recorded, categorising the activities in a way suitable for the habitual activity pattern of the population. As the activity categories differ, it is not possible to directly compare results between different studies.

Longitudinal time-motion studies have been carried out in two developed countries: Scotland (Durnin et al, 1987) and The Netherlands (van Raaij et al, 1990a). Activities were recorded by the subjects themselves during five consecutive days within each stage of pregnancy.

The Scottish women reduced the time they spent in bed during pregnancy ( - 30 min/day). At the end of pregnancy they spent more time sitting (+20 min/day) and less time walking ( - 30 min/day). There was no clear pattern of change in other activities with little indication that any marked diminution in activity occurred.

The Dutch women spent more time in bed (+70 min/ day), on very light sitting activities (+55 min/day) and on moderate household and walking activities (+25 min/day) during pregnancy. This was compensated for by spending less time on light and moderate sitting activities ( - 60 min/day) and on light standing activities ( - 90 min/day). In another Dutch study (Spaaij, 1993) women also spent more time in bed during pregnancy ( + 60 min/day).

In van Raaij's study an attempt was made to account for the combined effect of changes in both time allocation and in work intensity. Within each measurement period the energy cost of at least one activity from each category was measured. PALs were estimated by combining the energy expenditure results with the time allocated. At different stages of pregnancy, PAL was relatively constant (1.49-1.52) and the average during pregnancy (1.50) was only slightly below the value at 1 year post partum (1.53). The method has some clear drawbacks. Since the activities chosen for individual women were kept the same throughout the study there Ö was no accounting for changes in the choice of activities within each category. Furthermore it was assumed that the change in work intensity of the activity used for the measurement of energy expenditure was representative of the activities in each category.

In studies from developing countries, activities are not recorded by the subjects themselves, but by trained field assistants. In a longitudinal study conducted in Thailand (Thongprasert et al, 1987) women spent less time on childcare ( - 23 min/day), sitting, ( - 12 min/day), housework ( - 7 min/day) and walking ( - 6 min/day) and more time on agricultural tasks (+31 min/day) in late pregnancy compared to baseline estimates at 10 weeks gestation. Although there was a decrease in most activities, this was not compensated for by more time spent sleeping ( + 5 min/day).

In a longitudinal study conducted in The Philippines (Tuazon et al, 1987) activity diaries were only kept over 12 h and no real sleep/lying down/resting data was included. On average women spent more time sitting (+13 min/day), Iying down (+12 min/day) and on light housework (+17 min/day) during late pregnancy. This compensated for less time spent on moderate ( - 22 min/ day) and heavy housework ( - 26 min).

In The Gambia (Lawrence & Whitehead, 1988) women spent more time in bed during pregnancy (+30 min/day on field days and +60 min/day on home days) and less time on light/moderate housework ( - 40 min/day on both field and home days). However, on field days the duration of agricultural work (including walking to the fields) was not significantly affected by pregnancy and the major changes were decreases in the duration of household work ( - 20 min/ day) and walking around the village ( - 20 min/day). In another Gambian study (Roberts et al, 1982) activity was reported as total minutes/day spent on farmwork, housework, religious practices and walking. The times averaged 564 min/day at baseline (NPNL) and 493 min/ day when pregnant. Activity was generally lower during pregnancy than NPNL but peaked at four months and then decreased steadily to 407 min/day at nine months pregnant.

In a cross-sectional study conducted in Nepal (Panter-Brick, 1993), measurements were made over 12 h, so again there are no real sleep data. Pregnant women spent less time on outdoor activities including agricultural tasks ( - 23 min/day), husbandry ( - 22 min/day), forest work ( - 8 min/day), travel ( - 15 min/day) and rest ( - 5 min/day). This was compensated for by spending more time on indoor activities including domestic work (+34 min/day), family care (+10 min/ day) and rest ( + 41 min/day).

Durnin (1991) has pointed out that relatively small changes in activity patterns could result in significant energy savings. A calculated example shows that replacement of periods spent standing (60 min/day), on housework (30 min/day) and walking (30 min/day) by sitting; or by replacing sitting (60 min/day) by Iying down, could together result in an energy saving of about 700 kJ/day (165 kcal/day) or l95 MJ (45000 kcal) over the whole of pregnancy. However, the time-motion studies from developed countries do not show a consistent shift of time allocated to activity categories with high to those with lower energy costs. For example, both studies from The Netherlands showed an increase ( + 60 min) in the time spent in bed or Iying down, whereas the Scottish women reduced the time spent in bed ( - 30 min per day). Clearly, each category except 'Iying down' comprises a variety of activities, which could be performed at different intensities, and thus could involve a broad range of energy costs. During pregnancy, both the type and the intensity of activities within a category could change, resulting in energy savings without changes in the time allocated to different categories of activity. Therefore, although the longitudinal time motion studies presented above provide the best information available, they do not give conclusive data on how much energy is saved by changing activity patterns during pregnancy.

We conclude that it is reasonable to assume that about half the energy costs of pregnancy (i.e. about 0.6 MJ/day or 145 kcal/day) could theoretically be spared by reductions in the physical activity of the mother. However, it is difficult to uncover any patterns which could be described as typical pregnancy-induced behaviour. This emphasises that it cannot be assumed that a high proportion of energy costs of pregnancy are normally or automatically met by reductions in activity. The extent to which this occurs varies greatly among populations and individuals.

Energy cost of pregnancy: change in total energy expenditure

Total daily energy expenditure can be measured with whole-body calorimetry or the doubly-labelled water method. Studies using both methods are reviewed. Whole-body calorimetry allows detailed short-term measurements of 24 h energy expenditure (CalEE) and its components, but the respiration chamber is an artificial environment and the utilisation of strict protocols makes no allowance for behavioural changes. With the doubly-labelled water method the average total free living energy expenditure (TEE) can be measured over comparatively long periods of time (typically 10-21 days) without any hindrance to the subject.

Studies in which measurements of CalEE or TEE were carried out in combination with BMR measurements yield particularly useful data because energy expended on physical activity and thermogenesis can be calculated (CalEE-BMR or TEE-BMR). PALs can also be calculated from these data (CalEE/BMR or TEE/ BMR). BMR and RMR measurements are all referred to as BMR.

Respiration chamber studies. To date only five studies have been published in which assessments of changes in energy expenditure during pregnancy have been made by whole-body calorimetry. Three studies have been conducted in well-nourished Swiss (Schulz et al, 1988), British (Prentice et al, 1989) and Dutch (de Groot et al, 1994) women, two in marginally nourished women from The Gambia (Heini et al, 1992; Poppitt et al, 1993). The study by Heini et al, was cross-sectional. Calorimeter protocols differed between studies, but can all be classified as very sedentary.

Because of the different protocols and subject characteristics it is not surprising that, expressed on an absolute basis, CalEE differed between studies. Initial values varied from 6.2 MJ/day or 1480 kcal/day (The Gambia; Poppitt et al, 1993) to 8.3 MJ/day or 1980 kcal/day (Switzerland; Schutz et al, 1988). Changes in CalEE during pregnancy are presented in Figure 6. Four studies demonstrated a very consistent pattern of changes during pregnancy (de Groot et al, 1994; Heini et al, 1992; Prentice et al, 1989; Schutz et al, 1988). Increases in CalEE averaged 0.18, 0.41 and 1.26 MJ/day (43, 98 and 301 kcal/day) in the first, second and third trimesters of pregnancy, respectively. However, in the longitudinal Gambian study (Poppitt et al, 1993), CalEE decreased slightly in the first and second trimesters, and in the third trimester only increased by 0.15 MJ/day (36 kcal/day). This study involved marginally nourished women, which might explain the discrepancy (see earlier discussion of BMRs). In contrast, the cross-sectional study (Heini et al, 1992), carried out in the same Gambian villages, showed a pattern of changes that was rather more similar to those found in developed countries. However, the difference in weight between late-pregnant and non-pregnant women in Heini's study was 11.8 kg, nearly twice the weight gain observed by Poppitt (6.8 kg), indicating that the groups probably had different non-pregnancy body weights, and hence, different baseline CalEE values.

CalEE-BMR showed only minor changes during pregnancy: two studies showing a small increase and two other studies a small decrease. Expressed in this way, the results of Poppitt et al, (1993) deviate to a much lesser extent from the average. Apparently, the changes in CalEE during pregnancy were caused largely by the change of BMR.


Figure 6
Changes in CalEE measured by whole-body calorimetry during pregnancy. Closed triangles, Schutz et al, 1988; closed circles, Prentice et al, 1989; open circles, Heini et al, 1992; open squares, Poppitt et al, 1993; closed squares, de Groot et al, 1994. Solid line mean of all studies; dashed line mean excluding Poppitt et al (1993).

PALs were very constant fin two studies (Heini et al, 1992; Prentice et al, 1989) and a minor decrease was observed in the other two studies (de Groot et al, 1994; Poppitt et al, 1993). Doppler and actometer counts in de Groot's study confirmed that physical activity had somewhat decreased (Doppler counts - 6% and actometer counts - 17%).

We conclude that the CalEE of pregnant women increases steadily during pregnancy to a level about 1.5 MJ/day (360 kcal/day) higher than NPNL if activity remains constant. Most of this change is accounted for by the increase in BMR.

Doubly-labelled water studies. Six studies have reported measurements of TEE using the doubly-labelled water method. Four have been conducted in well-nourished women, from Britain (Goldberg et al, 1991; Goldberg et al, 1993), Sweden (Forsum et al, 1992) and the USA (Bronstein et al, in press) and two in marginally nourished women from The Gambia (Heini et al, 1991; Singh et al, 1989). Data from longitudinal studies (Forsum et al, 1992; Goldberg et al, 1991; Goldberg et al, 1993) and cross-sectional studies (Bronstein et al, in preparation; Heini et al, 1991, Singh et al, 1989) are presented together because of the small number of studies. All three longitudinal studies included pre-pregnancy baseline measurements.

Average non-pregnancy TEE values varied from 9.1 MJ/day to 10.4 MJ/day (2170 to 2480 kcal/day) in all normal weight groups of women; however, the TEE of the obese women (Bronstein et al, in preparation) was considerably higher (12.1 MJ/day or 2890 kcal/day). Changes in TEE are presented in Figure 7. These were more variable than changes in CalEE because physical activity accounts for a substantial and highly variable part of energy expenditure in normal daily life, but not under respiration chamber conditions. Average changes during pregnancy in normal weight women from developed countries were 0.11, 0.47 and 1.15 MJ/day (26, 112 and 275 kcal/day) in the first, second and third trimesters, respectively, which compares surprisingly well with the changes observed in respiration chamber studies (0.18, 0.41 and 1.26 MJ/day). However, the late pregnant increase in TEE in both of the longitudinal studies with more than two measurements (Forsum et al, 1992; Goldberg et al, 1993) was about 2 MJ/day (480 kcal/day). This deviates substantially from the cross-sectional studies in which the average difference between late-pregnant and non-pregnant women was only 0.4 MJ/day or 95 kcal/day (Bronstein et al, in preparation; Heini et al, 1991, Singh et al, 1989). The TEE results of the two longitudinal studies were at variance if the mid-pregnancy period was considered.

Changes in TEE-BMR are presented in Figure 8. It is apparent that changes in activity during pregnancy are highly variable between populations ranging between a reduction of - 1.2 MJ/day and an increase of + 1 MJ/ day ( 285 and + 240 kcal/day). The increases were observed in the two main longitudinal studies, and unchanged or decreased values in the cross-sectional studies.

High initial PALs (1.8 and 2.0) were observed in both Gambian studies (Heini et al, 1991; Singh et al, 1989) which agrees with the very active lifestyle of these women and the fact that measurements were made during the period of peak agricultural activity. The Swedish women, who the authors stated were 'professionally active', also had a high initial PAL (1.80) (Forsum et al, 1992). In the English and American studies (Bronstein et al, in preparation; Goldberg et al, 1991; Goldberg et al, 1993) the average non-pregnant PAL ranged between 1.58 and 1.66.


Figure 7
Changes in total energy expenditure (TEE) measured by doubly-labelled water during pregnancy. Closed circles, Singh et al, 1989; open circles, Goldberg et al, 1991; open squares, Forsum et al, 1992; closed squares, Heini et al, 1992; crosses, Goldberg et al, 1993; open triangles, normal weight, closed triangles, obese Bronstein et al, in preparation. Solid line, mean from developed countries normal weight; dashed line, mean from all studies (normal weight).


Figure 8
Changes in physical activity and thermogenesis (TEE-BMR) in free living women during pregnancy. References and symbols as Figure 7.


Figure 9
Changes in physical activity level (PAL, TEE/BMR) during pregnancy. References and symbols as Figure 7.

The cross-sectional studies generally found lower PAL values in pregnant vs non-pregnant women (Figure 9). In the longitudinal studies PALs at the end of pregnancy were below the pre-pregnancy baseline; in mid-pregnancy however, either an increase (Goldberg et al, 1993) or a decrease (Forsum et al, 1992) was observed.

We conclude that on average doubly-labelled water studies indicate very similar increases in TEE to those recorded in calorimeters (up to about + 1 MJ/day or +240 kcal/day towards term). There is a large variability between studies all of which have rather small samples. The two longitudinal studies show the largest increases (up to about + 2 MJ/day towards term). These new findings must be considered when trying to resolve the high requirements/low intake paradox. A steady decrease in PAL can be assumed to occur in affluent women as pregnancy progresses (to about --0.15 units at term). Note the PAL would decrease even if activity remained constant because the denominator (BMR) increases in pregnancy. If a PAL × BMR system is adopted for pregnancy, this observed decrease can be cited as the likely behaviour of well-nourished women. It will have to be stressed however that many women may not be able to decrease activity.

Energy supply during pregnancy: changes in energy intake

A substantial amount of data has been collected on changes in energy intake (EI) during pregnancy. The general observation is that the incremental intake during pregnancy does not meet the energy needs. In this section, eleven studies in which changes in EI were studied longitudinally during pregnancy are reviewed and critically re-examined. Studies were included if they described three or more stages of pregnancy relative to baseline.


Figure 10
Changes in energy intake during pregnancy. Left-hand panel, pregnancies resulting in average birthweight < 3kg: Squares, The Philippines, n = 40 (Barba, 1994); triangles, Thailand, n = 41 (Thongprasert et al, 1987); circles, The Philippines, n = 41 (Tuazon et al, 1987). Dashed line represents the mean. Right-hand panel, pregnancies resulting in average birthweight > 3kg: Closed triangles, Mexico, n = 45 (Allen et al, 1992); open triangles, USA, n = 95 (Bear, 1971); closed circles, England, n = 69 (Doyle et al, 1982); open circles, Scotland, n=81 (Durnin, 1991); open squares, England, n = 11 (Goldberg et al, 1993); closed squares, France, n = 437 (Papoz et al, 1982); large crosses, The Netherlands, n = 43 (van Raaij et al, 1987); small crosses, The Netherlands, n = 26 (Spaaij, 1993); asterisks, Australia, n = 49 (Trusswell et al, 1988). Dashed line represents the mean.

Changes in EI during pregnancy are shown in Figure 10. Studies with average birthweights <3kg (left-hand panel) are presented separately from those with more favourable average birthweights (right-hand panel). The observed average changes in EI during pregnancy varied dramatically. As shown in Figure 11, cumulative values ranged from - 0.59 MJ/day ( - 140 kcal/day) in The Phillippines, (Barba, 1994) to + 1.13 MJ/day (+270 kcal/day) in Thailand, (Thongprasert et al, 1987). In populations with average birthweights >3kg, the average increase in EI was 0.14, 0.38 and 0.42 MJ/day (33, 91 and 100 kcal/day) in the three trimesters of pregnancy, or on average only 0.31 MJ/day (74 kcal/day) over the whole of pregnancy.

It can be concluded that the reported EI of well nourished women shows a surprisingly small increase during pregnancy.


Figure 11
Average cumulative changes in energy intake during pregnancy. References as Figure 10.


Figure 12
Measured energy intakes of pregnant or lactating vs non pregnant European, North-American and Australian women, assumed to be eating to appetite. References as Figure 10.

Discrepancy between longitudinal and cross-sectional studies. Figure 12 summarises data on measured EI in groups of pregnant European, North American and Australian women, assumed to be eating to appetite. From cross-sectional comparisons, the average EI of pregnant women appears to be about 0.9 MJ/day (210 kcal/day) higher than those of NPNL women. This increase is substantially larger than observed in the longitudinal studies. The discrepancy implies that estimates from cross sectional studies are too high or estimates from longitudinal studies are too low. However, the cross-sectional comparison provides only a very crude estimate of changes in EI during pregnancy. An overestimation in the cross-sectional comparison could be caused by differences in EI estimates provided by populations of NPNL and pregnant women, but there is no reason to predict any particular directional bias from this source. However, the possibility of underestimation with longitudinal comparisons should also be considered.

Estimated changes in EI from longitudinal studies could be too low, if the simple fact of repeating the measurement affects the degree of under-reporting (for instance due to decreasing compliance as subjects tire of the procedure). This possibility was evaluated in two different ways: firstly studies which included post-lactational baseline measurements were compared with those which included pre-pregnancy baseline measurements; secondly, to test for decreasing compliance, repeated EI measurements in NPNL subjects were reviewed.

All the longitudinal studies presented in Figures 10 and 11 had pre-pregnancy or early-pregnancy baseline measurements. Such studies would provide too low estimated changes in intake, if under-reporting increased when the measurements were repeated: however, the same shift in validity would result in an over-estimation of changes in energy intake if post-lactational estimates were used as the 'baselines'.

Black et al, (1986) studied EI during pregnancy relative to a post-lactation baseline (3 months after weaning) in 46 women. EI averaged 8.8 MJ/day (2100 kcal/day) during the third trimester and 7.9 MJ/ day (1890 kcal/day) post-lactation. The average pregnancy value was 0.7 MJ/day (170 kcal/day) higher than the baseline. This is larger than the difference observed in the studies with pre-pregnancy baseline measurements (0.3 MJ/day) and supports the possibility of increasing under-reporting when repeating the measurement. However, as mentioned by the authors, dieting behaviour might also have caused the relatively low EI in the post-lactation period.

Goldberg et al (1991) found that the EI of ten women was 0.4 MJ/day (95 kcal/day) higher at 36 weeks gestation (9.8 MJ/day or 2340 kcal/day) than post partum (3 months after weaning) (9.4 MJ/day or 2245 kcal/day). This increase is identical to the average third trimester increase observed in studies with a pre-pregnancy baseline measurement.

King et al (1972), measured the EI of 14 to 17-year-old adolescents at 32 weeks gestation (7.8 MJ/day or 1860 kcal/day) and after delivery (7.0 MJ/day or 1670 kcal/day). The difference between the third trimester measurement and the post-partum baseline value (0.8 MJ/day or 190 kcal/day) is larger than the average difference in studies with pre-pregnancy baseline values, but adolescents may have a greater inherent need to increase their intake.

These studies provide little support for the contention that the low intakes observed during pregnancy may be due to measurement fatigue. At most this might be responsible for an error of about 0.2 MJ/day (48 kcal/ day) (derived by comparing the 0.8 MJ/day increment from the Black and King studies with the 0.4 MJ/day increment summarised above).

The possibility of increasing under-reporting when repeating EI measurements, was also evaluated using studies of repeated measurements of EI in NPNL subjects. Only studies in which measurements were repeated within 6 months were considered of interest.

Repeating 3- to 7-day weighed records resulted in a decrease of estimated EI in six studies, and in an increase in three studies. The weighted average of the change in EI relative to the baseline was - 0.2 MJ/day. Repeating 24-h recalls or food frequency questionnaires showed a decrease in estimated EI in three out of four studies. The weighted average of the change relative to the baseline was also - 0.2 MJ/day.

We conclude that there is reasonable evidence to suggest that the 0.3 MJ/day increment in EI observed in longitudinal dietary studies may underestimate the true change, but only by about 0.2 MJ/day. Over the whole of pregnancy this would raise the extra energy intake from 84 MJ to 140 MJ (20 000 to 33 500 kcal).

Recommendations for pregnancy

We recommend one of two possible methods of expressing the energy requirements of pregnancy. The first is a new proposal which extends the philosophy of using PAL values into pregnancy. The second is in line with the 1985 recommendations which simply refer to fixed increments, with optional reductions if activity is reduced.

Method 1: Expressing the energy requirements of pregnancy in terms of PAL values

The 1985 report treats pregnant women as non pregnant women with special incremental needs for energy deposition, and then makes some crude assumptions as to whether or not physical activity might alter. It could be argued that this misses an opportunity since the whole concept of recommendations based on PALs was designed to allow for differences in activity between groups of people and could logically be extended into pregnancy. There would be several theoretical advantages to unifying the methods of expression in this way, particularly as any assumptions about behavioural decreases in physical activity during the reproductive cycle could then be incorporated into the recommendations in a more formalised and explicit manner. We explored the possibility of using such an approach and recommend that its merits be considered.

We commented above that the Schofield equations cannot be used to accurately predict BMR during later pregnancy, but that fixed increments to the NPNL BMR could be proposed on the basis of the marked similarity between changes in BMR observed in well nourished women (see Figure 1). Additions of 0.2, 0.4 and 1.1 MJ/day were proposed for each trimester.

The use of PALs is somewhat complicated during pregnancy because BMR, the denominator in the calculation, increases over time. This means that a woman expending the same amount of energy on activity (TEE-BMR-DIT) throughout pregnancy would have a progressively decreasing PAL. If we take an example of a woman who performed exactly the same number of activities for the same duration and at the same intensity, PAL values would decline. This is because the energy cost of activity would only increase by about 10% in the last trimester (due to the mixed influence of weight-bearing and non-weight-bearing activity), whereas BMR would increase by 20%. The decline in PAL would also be greater in a more active woman. These changes are illustrated in Table 6 for hypothetical women and show that these theoretical objections to using PALs in pregnancy are not very significant in practice. Analogous objections can be raised to their use in obese subjects and these have been tolerated by previous expert committees.

Table 6 Examples to illustrate how PAL declines during pregnancy even if activity remains constant


Inactive affluent woman

Active developing country woman


NPNL

P3a

P3b

NPNL

P3a

P3b

BMR (MJ)

5.50

6.60

6.60

5.50

6.60

6.60

DIT (MJ)

0.85

0.85

0.85

1.10

1.10

1.10

TEE-BMR-DIT (MJ)

2.18

2.18

2.40

4.40

4.40

4.84

TEE (MJ)

8.53

9.63

9.85

11.0

12.1

12.54

PAL

1.55

1.46

1.50

2.00

1.83

1.90

'Error'


0.09 (6%)

0.05 (3%)


0.17 (9%)

0.10 (5%)

a Assumes that the net cost of activity remains unchanged.
b Assumes a 10% increase in net cost of activity.

If this approach is adopted it would need to be combined with a statement indicating that PALs do appear to decrease by about 0.1-0.2 units, at least in affluent women, as pregnancy progresses. For women in developing countries the obligatory nature of agricultural labour may remove opportunities for energy-sparing decreases in activity and PALs may remain constant (cf. Singh et al, 1987). The approach suggested here would readily accommodate such differences in behaviour and would highlight the fact that the energy requirements of pregnancy are only low if physical activity is reduced.

A complete rationalisation of the energy requirements of pregnancy in terms of PALs would require that the energy deposited be expressed as a PAL increment (i.e. as a multiple of BMR). This would only be possible if the required energy for deposition was known to be proportional to BMR, which is not the case. Such a procedure would be particularly flawed if the US recommendations (Nutritional Status and Weight Gain During Pregnancy, 1990) for differential weight gains according to initial BMI are adopted, because we would be recommending that thin women (with low BMRs) should gain more tissue (with a greater cost of deposition). This would require a whole set of PAL increments and thus be impractical. We recommend the use of fixed increments for energy deposition of 0.4, 0.7 and 0.5 MJ/day as discussed earlier.

Examples of the proposed approach. Table 7 illustrates two examples of how energy requirements in pregnancy can be estimated using PALs. The great advantage of such an approach is that it separates out the obligatory costs of pregnancy from possible energy-sparing adjustments, and therefore emphasises the fact that the energy requirements of an optimal pregnancy are high and must be met either from the diet or by decreasing activity.

Method 2: expressing energy requirements of pregnancy in terms of fixed increments

This approach is the same as employed in the 1985 report, but quantitatively updated to incorporate the large amount of new information available.

Figure 13 combines all the data from well-nourished women reviewed in previous sections to build up a picture of the energy needs of an average optimal pregnancy by summing the costs of maintenance, energy deposition, increased DIT and the passive increase in the cost of weight-bearing activity. This figure assumes that there is no change in activity pattern from NPNL. The average costs by trimester are 0.40, 1.10 and 1.80 MJ/day (96, 265 and 430 kcal/day), respectively. The total cost is 308 MJ (73 600 kcal). This is very similar to the estimate used in the 1985 recommendations.

Table 7 Examples of how to calculate energy requirements in pregnancy from pregnancy PAL values

Trimester

1

2

3

Well nourished affluent (MJ/day)a

NPNL BMRb

5.50

5.50

5.50

Pregnancy increment in BMR

0.20

0.40

1.10

Estimated PAL value

1.55

1.45

1.40

Total energy expended

8.83

8.56

9.24

Energy deposited

0.40

0.70

0.50

Total requirement

9.23

9.26

9.74

Daily increment over NPNL (assuming NPNL PAL = 1.6)

0.43

0.46

0.94

(Total cost of pregnancy = 170 MJ)




Poorly nourished developing country woman (NJ/day)a

NPNL BMRb

5.00

5.00

5.00

Pregnancy increment in BMR

0.20

0.40

1.10

Estimated PAL value

1.90

1.90

1.90

Total energy expended

9.88

10.26

11.59

Energy deposited

0.40

0.70

0.50

Total requirement

10.28

10.16

12.09

Daily increment over NPNL (assuming NPNL PAL = 2.0)

0.28

0.96

2.09

(Total cost of pregnancy = 310 MJ)




a All values are hypothetical and for illustrative purposes.
b Calculated by applying Schofield formula (1985) to average NPNL body weight for populations in question.

Figure 14 uses the same data as in Figure 13, but plots them relative to the average observed increase in EI in affluent pregnant women. The average costs by trimester for such pregnancies are, by definition, equal to the observed increase in intake and are 0.14, 0.38 and 0.42 MJ/day, respectively, or 0.3 MJ/day over the whole of pregnancy. The total cost would be 84 MJ (or 140 MJ if we allowed for potential progressive under-reporting in longitudinal studies). Another way of arriving at this figure is to add up the total costs of each component over the whole of pregnancy as:

S ECONCEPTUS + SEFAT + SEMAINTENANCE where SECONCEPTUS = 42 MJ or 10 000 kcal (includes 400 g fetal at); SEFAT = 2.5 kg × 39 kJ/g = 98 MJ (23400 kcal); and SEMAINTENANCE = 160 MJ (38 000 kcal).


Figure 13
Aggregated energy costs of pregnancy if physical activity remains unchanged. Clear area, energy deposited, shaded area BMR dark area, DIT; hatched area, physical activity: area 1 = PAL of 1.55, areas 1 + 2 PAL of 2.00.


Figure 14
Aggregated energy costs of pregnancy plotted in relation to observed increases in energy intake in well-nourished women. Hatched area, energy deposited; shaded area, BMR; dark area, DIT; horizontal stripes, physical activity if NPNL PAL (1.55) remains unchanged; stippled area, physical activity if NPNL PAL (2.00) remains unchanged.

This gives a total of 300 MJ (71 700 kcal) equivalent to 1.07 MJ/day (255 kcal/day) (rounded to 1.1 MJ/day).

Both of these values are considerably less even than the lower 1985 recommendation which is conditional on women reducing their activity. The lower edge of the hatched area in Figure 14 indicates the extent to which physical activity must be reduced in order to accommodate the obligatory costs of pregnancy within such a small increase in intake.

Lactation

In general there is much less new information concerning the energy requirements for lactation than there is for pregnancy, but this is offset by the fact that the basis for computing recommended intakes is more straightforward. The energy costs of lactation are customarily calculated as: [NPNL requirements] + [Breastmilk volume × Energy density × Conversion efficiency] ± [Change in body fat] ± [Changes in activity]. Possible changes in maternal metabolic rate and DIT can either be incorporated into the factor describing 'conversion efficiency', if this is expressed as gross efficiency, or may be dealt with as a separate category added to the above scheme. The following sections summarise the available quantitative data on each component.

Energy cost of lactation: energy output in breast milk

Volume of milk produced. Figure 15 illustrates that the volume of milk produced at peak lactation is remarkably similar in groups of women from a wide variety of nutritional and cultural circumstances.* For a previous IDECG report we demonstrated that lactational performance does not appear to be compromised by low BMI (Prentice et al, 1994). It therefore appears that even small, undernourished women produce similar amounts of milk to larger, well-nourished women. Consequently there is little difficulty in arriving at acceptable average values for milk production in early lactation. The values selected by the UK Expert Panel (COMA, 1991) were derived as the average of two of the most carefully conducted series of measurements. The data were from well-nourished women from England (Paul et al, 1988) and Sweden (Sadurskis et al, 1988) and incorporated a 4% correction to allow for insensible water losses by the infant during test-weighing. In Table 8 we have combined these with data from the Californian DARLING Study (Heinig et al, 1993a; 1993b; KG Dewey, personal communication). These values are broadly representative of other populations. They are slightly lower than the 1985 figures particularly for 3-6 months post partum. The values after 6 months of lactation in Table 8 are a rough approximation based on the 1985 figures supplemented by data from other studies of extended lactation (Prentice et al, 1986).


Figure 15
Similarity of breast-milk output in groups of women from different nutritional and cultural settings. Reproduced permission from (Prentice et al, 1986). Data are from 1118 women in 26 studies.

In later lactation the quantity of milk produced is largely dependent on cultural practices and on the mother's intentions concerning weaning. The UK Panel adopted two different sets of figures: (a) for women 'who practice exclusive or almost exclusive breast-feeding until the baby is 3-4 months old and then progressively introduce weaning foods as part of an active weaning process' and (b) for women 'who introduce only limited complementary feeds after 3-4 months and whose intention is that breast-milk should provide the primary source of nourishment for 6 months or more'. Making a distinction between partial and full breast-feeders in this way is worth considering, but would have to be made more general for a WHO document. In Table 8 the figures for partial breast-feeders have simply been set as 50% of the output of full breast-feeders.

*Note that although more modern data are available than summarised in this figure they tend to fit the same pattern and a fresh analysis was not considered necessary.

Energy content of breast milk. It is notoriously difficult to obtain a truly accurate estimate of the energy density of breast milk transferred from the mother to her infant. This is because complex diurnal, within-feed and between-breast changes in milk fat content make it virtually impossible to design a sampling protocol which will yield an integrated estimate of energy density over the whole day and in a manner which will not affect the natural pattern of milk flow. Once milk has been sampled, the energy content has usually been calculated by applying modified Atwater factors to chemical estimates of the proximate constituents.* A large government survey in the UK reported average metabolisable energy of mature milk to be 2.90 kJ/g (0.69 kcal/g) equivalent to a gross energy (GE) content of 3.06 kJ/g (0.73 kcal/g) (DHSS, 1977). This agrees exactly with estimates from the WHO multi-centre collaborative study on breast-feeding. Direct estimates of the GE content of pooled milk from well-nourished women has yielded a value of 3.10 kJ/g (0.74 kcal/g) which is also in close agreement (Garza & Butte, 1986). Many other studies yielding similar values could be quoted.

* Note that this calculation incorporates estimates of digestibility for protein, fat and carbohydrate. It therefore represents metabolisable energy available to the child, but underestimates the gross energy which must be provided by the mother (the difference appears in the infant's stools). This represents a clear error in the WHO/FAO/UNU (1985) assumptions and should be corrected even though the impact of the change is not large.

Table 8 Suggested breast-milk volumes for use as basis of calculations

Months

Proposed volumesa

1985 valuesb

All women

0-1

680

719

1-2

780

795

2-3

820

848

Full breast-feeders

3-6

830

822

6-12

650

600

12-24

600

550

Partial breast-feedersc

3-6

415

Not applicable

6-12

325

Not applicable

12-24

300

Not applicable

a Derived from studies in Sweden (Sadurskis et al, 1988) England (Paul et al, 1990), USA (Heinig, 1993a,b) and the WHO Collaborative Study on Breast-Feeding (WHO, 1985). Values are g/d and include a 4% correction factor to allow for insensible water losses from the baby during test-weighing.
b Derived only from the WHO Collaborative Study on Breast Feeding. Values are g/d.
c Infants receiving breast-milk as only source of milk.

An alternative approach has been employed in an attempt to assess the energy content of breast milk indirectly from measurements of energy expenditure and from the composition of new tissue formed in breast-fed infants (Lucas et al, 1987). It is claimed that this gives a more representative picture of milk as suckled by the infant, but the method necessitates a number of assumptions and has not been independently validated. Its results are therefore viewed with some caution (COMA, 1991). Using this approach the calculated metabolisable energy in early lactation was 2.40-2.50 kJ/g (0.57 - 0.60 kcal/g). This should be increased by 5% (to about 2.55 kJ/g or 0.61 kcal/g) to obtain GE.

A consideration of the energy content of milk from under-nourished mothers is not strictly relevant to the formulation of recommended dietary allowances since these should cover optimal milk quality. Nonetheless it is worth noting that, in spite of some reports to the contrary, the consensus of opinion is that milk energy holds up very well in the face of maternal under-nutrition. Several reviews are available (Ferris & Jensen, 1984; Jensen & Neville, 1985; Neville & Neifert, 1983). Our own earlier analysis of relationships between maternal BMI and milk energy content reported that there were three studies in which there was a significant positive association between the two variables, but that most revealed no association and at least one showed a reverse trend (Prentice et al, 1994).

The choice of a figure for the energy content of milk should lie somewhere between 3.00 kJ/g or 0.72 kcal/g (average GE from proximate analysis or bomb calorimetry of pooled mature milk) and the new estimate of 2.55 kJ/g (Lucas et al, 1987). The 1985 value was 2.90 kJ/g, and the UK (COMA, 1991) adopted 2.80 kJ/g (0.67 kcal/g) as a compromise. We have used 2.80 kJ/g in the calculations below.

Efficiency of converting dietary energy to milk energy. The 1985 Report assumed a figure of 80% efficiency for milk synthesis. This was based on a study by Thompson et al (1970) and was derived as the lower 95% confidence interval of their individual estimates. The average apparent efficiency was in fact close to 100%. There are a number of serious problems with this derivation. These include the use of a cross-sectional design comparing lactating and non-lactating women; a heavy dependence on estimates of food intake in the mothers; an absence of any milk production measurements (milk energy transfer was estimated from the growth rate of the breast-fed infants and assumptions regarding the energy cost of growth); and an absence of estimates of changes in maternal fat stores. We argue below that the estimate of 80% efficiency should not be altered, but that alternative justifications for the figure should be adopted.

The efficiency with which a mother can convert dietary energy can be estimated in two ways: as biochemical efficiency or as calorimetric efficiency.. Both involve a number of assumptions and are therefore imprecise, but they provide a reassuring level of agreement.

Biochemical efficiency. It is possible to compute the biochemical efficiency of synthesising each of the proximate constituents of breast milk from the known stoichiometric equations and the obligatory heat losses associated with each step of the synthetic process. A full description is available elsewhere (Prentice & Prentice, 1988). The calculated efficiencies are 95% for lactose synthesis, 88% for protein synthesis, 73% for de novo fat synthesis; and 98% for transfer of pre-formed fat. Human milk is notable for the small proportion of fat which is synthesised (Hachey et al, 1989), even when women are consuming a low-fat diet. Most fat is assumed to be transferred from the diet, even if it is recycled (at a low biochemical cost) through adipose tissue. The overall efficiency of synthesis for all proximate constituents combined is therefore very high; averaging about 91-94%. This is much higher than in many mammals (especially ruminants) which are forced to synthesise a higher proportion of milk fat.

It is important to emphasise that these estimates of biochemical efficiency must represent the absolute maximum efficiency since they are derived from a gross simplification of the biochemical pathways involved. They make no allowances for the numerous other minor processes which are needed to support the synthetic process (Prentice & Prentice, 1988). Allowances must also be made for the further costs associated with digestion, absorption, interconversion, transport and storage of the dietary fuels and protein. These can probably best be assessed from direct measurements of DIT. Most studies report that 6-14% of the energy of a mixed meal is dissipated as heat (Jéquier & Schutz, 1985). Illingworth et al (1986) reported a 30% diminution of DIT during lactation. This figure is questioned below, but if it is accepted it would reduce estimates of thermogenesis to about 8% of any extra metabolisable energy ingested to support lactation. Adding this to the biochemical estimates for synthesis gives an overall efficiency of about 83%, which lends strong support to the assumption adopted in the 1985 report.

Calorimetric efficiency. An alternative approach to the theoretical calculations of biochemical efficiency outlined above is to perform metabolic balance studies which include calorimetric measurements of the maternal maintenance requirements. Calorimetric efficiency of milk production can then be computed as:


where the denominator is the sum of excess energy derived from the diet and by mobilisation of body fat stores, and-where the term 'maintenance needs' encompasses all components of energy expenditure including physical activity.

This method has been developed by livestock scientists and the literature is dominated by estimates from dairy cattle. Unfortunately there are few data from other species. Calorimetric efficiency in ruminants ranges from about 67-72% (Blaxter, 1962; Flatt & Moe, 1971). Some values from non-ruminants are: rat 57% (Roberts & Coward, 1982); rabbit 76% (Partridge et al, 1983); and pig 85% (Lodge, 1957). Humans are likely to lie towards the top end of this range due to the low level of fat synthesis.

Efficiency is known to vary with the state of maternal energy balance since mobilised body energy is used more efficiently than dietary energy. This is in accord with theoretical predictions based on the difference between transfer and synthesis costs for fats. The efficiencies of conversion of dietary and body energy have been calculated as 63% and 84% respectively in the dairy cow (Flats & Moe, 1971) and 74% and 94% in the rabbit (Partridge et al, 1983). In humans this difference is likely to be much less pronounced since the high fat content of the diet removes the need for substantial lipogenesis.

Recent calorimetry data from lactating women in The Gambia have been used to calculate a variant of calorimetric efficiency (Frigerio et al, 1991a). The study assumed that the extra costs of milk synthesis would be measured as part of BMR and computed efficiency as (%):


Based on cross-sectional measurements in lactating and non-lactating women, efficiency was found to be 94.2 ± 3.5%. It must be stressed that this value is not directly comparable with the livestock definition of efficiency which incorporates all components of daily energy expenditure in the denominator. It should also be noted that this approach assumes that milk synthesis is equally active during the measurement of BMR. This assumption may not be entirely correct since, by definition, the women are measured at the greatest distance from a previous meal. If milk synthesis (and hence its effect on BMR) diminishes in the fasted state this would tend to over-estimate efficiency.. Finally it should be noted that in previous longitudinal studies in the same population (Lawrence et al, 1986) BMR was actually lower in lactating women than prior to conception. In the above method of calculation this would yield an apparent efficiency in excess of 100%. The only way that this can occur is for other components of the maternal metabolism to be down-regulated to an extent which more than compensates for the known obligatory costs associated with synthesis. The need for physiological down-regulation seems to be caused by an inadequate diet and might have detrimental consequences to the mother. Such high apparent efficiencies should not therefore be used as the basis of recommended requirements. If BMR is not suppressed in lactating women (see below) this would lead to lower estimates of efficiency if calculated using the Frigerio formula.

Blaxter (1962) noted that calorimetric efficiencies are usually 10-15% lower than biochemical efficiencies. This is entirely to be expected from the known omissions in the biochemical estimates. Applying this correction to the estimate of biochemical efficiency derived above would yield a figure of 80-85%. Once again this is in accord with the figure used in the 1985 recommendations, and suggests that no change is needed.

Energy cost of lactation: change in basal metabolic rate

Introduction. It would be anticipated that the BMR of a lactating woman would be slightly higher than in her non-lactating state if, as is generally assumed to be the case, milk synthesis is a continuous process in humans and is active during measurements of BMR. The increase would be equivalent to the 'inefficiency' of the synthetic process (i.e. 20% if we accept the 80% estimate of efficiency).. At 3 months post partum this would be about 460 kJ/day (110 kcal/day) or around 10% of BMR (derived as 820 g × 2.80 kJ/g × 0.20). Any value lower than this would be indicative of energy-sparing.

There are fewer BMR data available for lactation than for pregnancy, and there is not such a clear consensus. An earlier review (Prentice & Whitehead, 1987) tentatively concluded that there was quite good evidence that BMR was lower during lactation than in the NPNL state (see Figure 16), and that this could represent significant evidence of energy-sparing when considered in the light of the expected rise in BMR explained above. However, this analysis included data from under-nourished women and more recent studies indicate the need for a reappraisal.

Studies from developed countries. The earliest studies from well-nourished women certainly suggested that BMR was suppressed (Johnston et al, 1937; Rowe & Boyd, 1932). The study by Rowe & Boyd involving a total of 77 women in Boston seems particularly convincing and illustrates a U-shaped depression in BMR coincident with peak lactation and reaching a minimum value 15% below the Harris-Benedict and Aub-Dubois standards. By 12 months post partum BMR was only 2-4% below the standards. Similar results were later obtained by Blackburn & Calloway (1985) who made RMR measurements in 13 lactating women at 8-12 weeks post partum. On average, RMRs were 23% lower than predicted, but these data should be treated with considerable caution since it is stated that the women were allowed to sleep during the measurement if they chose. Clearly both studies are handicapped by the fact that they compare BMR in lactation with predicted values rather than with true measurements in a non lactating state.

In contrast, no differences in RMR were found between breast- and bottle-feeding women in a cross sectional study in Scotland. When RMR was remeasured post-lactation in the breast-feeding women it was also unaltered (Illingworth et al, 1986). In a longitudinal study in Cambridge (Goldberg et al, 1991), BMR measured at 4, 8 and 12 weeks lactation (5887, 5846 and 5630 kJ/day or 1406, 1396 and 1345 kcal/day) was very similar to the post-lactation value (5858 kJ/day or 1399 kcal/day). When expressed per kg fat-free mass, the values (144, 145, 141 and 142 kJ/kg FFM/day) again indicated no suppression during lactation.

A longitudinal study of 40 lactating Dutch women is a little more difficult to interpret (van Raaij et al, 1991). At 9 weeks post partum, average BMR was 5940 kJ/day (1418 kcal/day) and at 12 weeks gestation was 6380 kJ/ day (1524 kcal/day), suggesting that BMR was 440 kJ/ day lower during lactation. A cross-sectional comparison using a matched group of 16 non-lactating women measured at 9 weeks post partum revealed no difference in BMR (average 5940 kJ/day or 1419 kcal/ day). On the basis of data in Figure 16, the 12 weeks gestation figure should be adjusted downwards by about 250 kJ/day (60 kcal/day) to represent pre-pregnancy BMR. The residual difference is small. Furthermore, longitudinal measurements at 5, 9, 13, 27 and 56 weeks post partum, in a subgroup of 16 of the 40 lactating women suggested that there was no influence of decreasing milk flow or weaning (6050, 6088, 5929, 6050 and 6042 kJ/day or 1445, 1454, 1416, 1445 and 1443 kcal/day respectively). In a more recent longitudinal study of 24 Dutch women (Spaaij et al, 1994a) mean RMR was 3.80 ± 0.35 kJ/min (0.91 ± 0.08 kcal/min) before pregnancy and 3.98 ± 0.40 kJ/min (0.95 ± 1.10 kcal/min) at two months lactation. The increase was statistically significant (p < 0.05), but represents less than a 5% change.


Figure 16
Analysis of changes in BMR during pregnancy and early lactation. Reproduced with permission (Prentice & Whitehead, 1987). (Basal)


Figure 16 Analysis of changes in BMR during pregnancy and early lactation. Reproduced with permission (Prentice & Whitehead, 1987). (Resting)

Increases in RMR during lactation were also observed in a longitudinal study of 23 Swedish women (Sadurskis et al, 1988). Post-partum RMR values were 6364, 5904 and 6029 kJ/day (1520, 1410 and 1440 kal/ day) at 5-10 days, 2 months and 6 months post partum, respectively compared to 5611 kJ/day (1340 kcal/day) before pregnancy. Breast-feeding patterns at 6 months post partum were not clear from the original publication, but all women were lactating at 2 months. At this time the increase in RMR above the pre-pregnancy measurement (314 ± 670 kJ/day or 75 ± 160 kcal/day) was significant (p < 0.05). Differences were also significant when expressed per kg FFM since, surprisingly, FFM was found to be appreciably lower in lactation (42.3 vs 45.0 kg, p < 0.05). As in Spaaij's study the difference only amounted to about +5%.

We conclude that in well-nourished women the most robust studies involving longitudinal measurements suggest that RMR is unchanged or only very slightly elevated in lactation.

Studies from less developed countries. There are much fewer studies from women in developing countries, but with one exception they support the data from developed countries. In Guatemala (Schulz et al, 1980) RMRs were similar in 18 lactating women (3.18 ± 0.42 kJ/min or 0.76 ± 0.10 kcal/min) and 6 non-lactating women (3.06 ± 0.54 kJ/min or 0.73 ± 0.13 kcal/min). In The Gambia, (Lawrence et al, 1986) BMR was about 420 kJ/day (100 kcal/day) lower in lactating women compared to their own pre-pregnancy baseline and, furthermore, BMR was lower in unsupplemented women than in those receiving an energy-dense dietary supplement. However, cross sectional comparisons conducted in the same villages yielded different results (Singh et al, 1987). Mean RMR was 5471 ± 776 kJ/day (1307 ± 185 kcal/day) in 15 lactating women and 5012 ± 130 kJ/day (1197 ± 31 kcal/ day) in six NPNL women; the differences were not significant. ln The Philippines, Guillermo-Tuazon et al (1992) found no significant difference between BMR measured during lactation and at 13 weeks gestation in the same 32 women.

Energy cost of lactation: change in diet-induced thermogenesis

Two longitudinal studies have been published on changes in DIT in response to a standardised liquid meal during lactation. lllingworth et al (1986) observed a significant ( - 30%) reduction in DIT during lactation, compared to post-lactational measurements in 12 women (0.42 vs 0.60 kJ/min or 0.10 vs 0.14kcal/min). However, in a longitudinal study of 24 Dutch women (Spaaij et al, 1994a), DIT at 2 months lactation was the same as the pre-pregnancy baseline measurement (0.64 kJ/min or 0.15 kcal/min).

DIT in lactating and non-lactating women has been evaluated in two cross-sectional studies. In both, the energy content of the test meal was larger in the lactating than in the non-lactating women, and therefore the results cannot be compared. Motil et al (1990) observed a highly significant 4.4-fold higher DIT (kcal/kg body wt/day), in 12 lactating women compared to nine non lactating women, whereas the energy content of the test meals used was only 1.5-fold higher. This result may be influenced by quite considerable differences in body composition. In a Gambian study DIT, expressed as a percentage of the energy consumed, in 10 lactating women (at 2 months post partum) was similar to that in 12 NPNL women studied during the same (dry) season (Frigerio et al, 1992). A second group of lactating women was studied during the rainy and nutritionally unfavourable season. DIT was lower ( - 18%) than in the lactating women studied in the dry season (p < 0.05), and lower ( - 16%) than in the NPNL control group (also studied in the dry season).

The results of these four studies are conflicting. There is no clear evidence that DIT is either increased or decreased during lactation. We will assume that it remains constant when expressed as a proportion of energy ingested.

Energy cost of lactation: change in energy costs of activity

Energy cost of standardised activity. Several investigators have studied the energy cost of cycle ergometer or treadmill exercise in lactating women (Blackburn & Calloway, 1974, 1976, 1985; Edwards et al, 1981; Knuttgen & Emerson, 1974; Lotgering et al, 1991; Pernoll et al, 1975; Seitchik, 1967; Spaaij et al, 1994a; Uleland et al, 1973; van Raaij et al, 1990b). However, it was not possible to perform an analysis of any potential effects of lactation because subject groups were not clearly defined. For example, in some studies which included data from post-partum women it was not stated whether or not they were lactating. In others, lactating and non-lactating women were treated as a single group and it was not possible from the information given in the original papers to sub-divide the groups.

Changes in activity patterns (time-motion studies). In a study by van Raaij et al (1990a), eighteen Dutch women with sedentary lifestyles were studied longitudinally and kept activity diaries at 5, 9, 13 and 27 weeks lactation and at 56 weeks postpartum when NPNL.

Compared to NPNL the time spent sitting quietly or whilst carrying out light activities was increased at 5 weeks lactation (+36%, from 345 to 470 min/day). The time spent on light/moderate sitting activities was ( - 48%) lower at 5 weeks lactation. Increases were observed from 9-27 weeks but values remained lower than NPNL. The time spent on standing/light standing activities was lower at 5, 9 and 13 weeks lactation whilst at 27 weeks they were very similar to NPNL. There was very little change in the times spent moderately active, walking and cycling. The amount of time spent on infant feeding progressively decreased between 5 weeks (145 min/day) and 27 weeks lactation (75 min/day). Very little time (5 min/day) was spent on recreational activities when NPNL and at 27 weeks lactation, and none at all at 5, 9 and 13 weeks. PALs calculated from these data were 1.47, 1.50, 1.48, 1.5;0 and 1.53 at 5, 9, 13, 27 weeks and NPNL, respectively. Net costs of physical activity were calculated to be 200 kJ/day (48 kcal/day) lower in lactating compared to NPNL women.

The findings by van Raaij et al, are broadly similar to observations from British women (Goldberg et al, 1991). The lower PALs in lactation, measured by doubly-labelled water (see below) compared to NPNL were substantiated by responses to interview questionnaires. All women reported being less active and more tired, especially during the first 4 weeks when more time was spent sitting and sleeping (not necessarily as a result of suckling) and only minimal time was spent on shopping or housework. Many women did not resume discretionary activities until 8 weeks post partum or later.

In a longitudinal study of lactating Swedish women, physical activity was assessed using activity diaries kept over 24 h (Sadurskis et al, 1988). Activities were classed into nine categories and assigned a multiple of BMR (FAO/WHO/UNU, 1985). The weighted average was used as an indicator of physical activity. Values were the same at two months lactation and before pregnancy (1.59 and 1.60, respectively). The women were considered to have sedentary lifestyles and the authors stated that interviews and questions concerning sports, strenuous work, mode of transport and sleeping habits corroborated the diary data. However, when doubly-labelled water data from these subjects were analysed (Forsum et al, 1992), the subjects were re-considered to have more active lifestyles (see below).

In a cross-sectional study in The Gambia (Roberts et al, 1982), activity records were made over 3-10h and activity recalls used to study activity patterns. The data were presented for the total time spent active during the day. Activities included farmwork, housework and religious duties and were very dependent on season. The stage of lactation did not affect the total time taken or activity levels when performing household tasks or light farming work, but did influence the level of activity during heavy farming. Levels of activity were also affected by whether or not the women were accompanied by their infants. Seasonally adjusted figures for 0-11 months lactation are shown in Figure 17. On average 564/min/day was spent on activities in NPNL women and 501 min/day in [lactating women. Activity was lowest at 1 month lactation (364 min/day), but this was due to the tradition of confinement to the family compound during this time. Levels gradually increased to NPNL levels (550 min/day) by 11 months lactation.

In a longitudinal study of 40 Philippino women 5-day activity records were made during pregnancy and lactation (Tuazon et al, 1986, 1987). Observations were only made over 12 h, so overnight sleeping, Iying or resting data are unavailable. 'Baseline' data were taken at 14 weeks pregnant. Light/moderate activities were carried out in the first few months, but then returned to more habitual heavy levels. As lactation progressed resting activities decreased and other activities increased, except for light housework which remained the same. There was no suggestion that physical activity was reduced. PALs were calculated as 1.61 and 1.80 at 6 and 12 weeks Lactation, respectively.


Figure 17
Time allocation data from lactating women in The Gambia. Taken from Roberts et al (1982).

In a cross-sectional study (Panter-Brick, 1993) conducted in Nepal, NPNL and lactating women (between 0 and 35 months) were compared. Activities were recorded by observers during two non-consecutive days. PALs (averaged across seasons) averaged 1.92 in NPNL and 1.80 in lactating women. Time allocated to different activities was highly dependent on season, and activity levels were not significantly different between NPNL and lactating women in periods of intense activity. The author concluded that the seasonal constraints on the women's work prevented them from significantly curtailing physical activity at these times and effectively limited the scope of behavioural mechanisms for saving energy to support lactation.

We conclude that although there is a limited number of studies and there are differences with respect to populations and study design there are some similar trends in the data.

In developed countries women tend to decrease total physical activity, especially with respect to moderate and discretionary activities. This is sometimes, but not always, associated with childcare, for example more time spent sitting. These reductions in activity do result in energy saving which may help to support the costs of lactation. However, in women whose activity levels are already low, the potential for such savings is limited. Conversely, in affluent, sedentary women, the increased demands of childcare may serve to increase energy expenditure. An important consideration is that women have to be economically and socially able to 'afford' to reduce physical activity, for example by giving up paid employment.

In developing countries, although activity levels are generally much higher and therefore the potential for savings by reducing expenditure are greater, in practice women cannot or do not reduce their activities during lactation. Usually where decreases have been observed this is due either to cultural practices (e.g. confinement) or seasonal effects.

As for pregnancy, we propose that any new recommendations should be very cautious about making assumptions about possible energy-sparing decreases in physical activity during lactation.

Energy cost of lactation: total energy expenditure

Respiration chamber studies. The only study which has reported data from 24 h whole-body calorimetry measurements of lactating women is that by Frigerio et al (1991b) The combined 24 h CalEE of Gambian mothers and their infants measured in 16 lactating women and 16 controls was 2.3 MJ/day (549 kcal/day) higher in the lactating women. The authors attributed 66% of this to the infant's energy expenditure (1.5 MJ/day or 358 kcal/ day) and 33% (0.8 MJ/day or 191 kcal/day) to increased spontaneous activity of the mother.

Doubly-labelled water studies. Only four studies have used doubly-labelled water to measure TEE in lactation. Two of these were longitudinal in British (Goldberg et al, 1991) and Swedish (Forsum et al, 1992) women. One was cross-sectional in Gambian women (Singh et al, 1989). One other study, conducted in the USA (Lovelady et al, 1993), measured energy expenditure only once in women between 12 and 26 weeks lactating who were either exercising or not exercising, but there were no measurements of non-lactating women.

Mean** TEE: values in NPNL women ranged between 9.8 MJ/day (2340/ kcal/day) (UK) and 10.8 MJ/day (2580 kcal/day) (Sweden). Figure 18 illustrates the effects of lactation on absolute TEE for all studies. TEE in Swedish and Gambian women was higher in lactation than NPNL, whereas in the UK women, there was a marked decrease, especially at 4 weeks. Mean changes ranged from increases of 0.42 MJ/day (100 kcal/day) at 20 weeks in Gambian women to decreases of 0.94, 0.69 and 0.83 MJ/day (225, 165 and 198 kcal/day) in British women at 4, 8 and 12 weeks, respectively. In their study with no NPNL controls, Lovelady et al (1993) found a mean TEE of 10.1 MJ/day (2410 kcal/day) at 12-26 weeks; in the middle of the range from the other three studies.

** Note that DLW estimates do not include the energy transferred in milk, but do include the biochemical costs of synthesis.

Energy expended on TEE-BMR averaged 5.1 MJ/day (1218 kcal/day) in the Gambian women, higher than both Swedish (4.7 MJ/day or 1123 kcal/day) and British (2.9, 3.2, 3.3 MJ/day or 693, 764 and 788 kcal/day) women. The Gambian values were slightly (0.1 MJ/day or 24 kcal/day) higher during lactation than NPNL. In contrast, there was a marked decrease in the mean values for the Swedish (0.5 MJ/day or 119 kcal/day) and British (0.98, 0.68, 0.60 MJ/day or 234, 162 and 143 kcal/ day) women.

PALs for both non-lactating and lactating Gambian women were very high averaging 1.98 and 1.97, respectively. This reflects the women's lifestyle and the fact that measurements were made at a period of peak agricultural activity. When non-lactating, the Swedish women also had high values averaging 1.94 (the authors described the women as 'professionally active') decreasing to 1.82 and 1.79 at two and six months lactation, respectively. The British women had more moderate levels of activity with PALs averaging 1.66 when non lactating. Values during lactation were markedly lower averaging 1.50, 1.56 and 1.59 and 4, 8 and 12 weeks lactation, respectively.


Figure 18
Total energy expenditure (TEE) measured by doubly-labelled water during lactation. Squares, The Gambia (Singh et al, 1989); triangles England (Goldberg et al, 1991); circles, Sweden (Forsum et al, 1992).

With only four studies and very different population groups and lifestyles. it is impossible to draw firm conclusions about changes in TEE during lactation. In women who are obliged to continue working, possibly at very high levels of physical activity, the energy costs of lactation need to be supported by body fat mobilisation or increased energy intake. In women who can afford to, energy costs may be partially met by decreases in energy expended on physical activity.

We conclude that there is insufficient data even to make qualitative statements about 'normal' changes in TEE during lactation. There is no clear evidence that activity is habitually decreased as an energy-sparing strategy.

Energy supply during lactation: change in energy intake

Numerous assessments of EI have been made during lactation. However the majority were cross-sectional studies, or longitudinal studies which did not include a pre or post-lactational baseline measurement (see Figure 12). Only studies of longitudinal food intake measurements with a pre-pregnancy, first trimester or post-weaning baseline have been included in this review (Allen et al, 1992; Black et al, 1986; English & Hitchcock, 1968; Guillermo-Tuazon et al, 1992; Prentice et al, 1986; Sadurskis et al, 1988; Schofield et al, 1987; Spaaij, 1993; van Raaij et al, 1991; Whichelow, 1975).

Figure 19 shows the longitudinal changes in EI during lactation in women from developed and developing countries. Whilst there are large differences, the majority of studies showed an increase of between 0.3 to 1.6 MJ/day (70 to 380 kcal/day). Three studies provided multiple estimates of EI during lactation, from which it is apparent that intake was highest during the first 3 months post partum and then gradually declined. Only the study of Scottish women (Schofield et al, 1987) suggested that EI falls slightly during lactation. Whichelow's study of English women (1975) shows greater increases than any of the other studies, except that of Allen et al (1992) in Mexican women. Whichelow's paper however does not describe the methods used for data collection and it is possible that the discrepancy is a result of inadequate methodology. The two outliers (Schofield et al, 1987; Whichelow, 1975) have been excluded from the average intake figures shown by the dotted line in Figure 19. The average increase in EI 3 months post partum, the time considered to be peak lactation, was 1.35 MJ/day (322 kcal/day) and 1.01 MJ/ day (241 kcal/day) in the developed and less developed countries, respectively.

The mean changes have been ranked in order of decreasing intake in Figure 20. This highlights the outliers which have been discounted. The remaining studies reported average changes of between 0.2 MJ/day (48 kcal/day) (Schofield et al, 1987) and 2.5 MJ/day (595 kcal/day) (Allen et al, 1992).

The average increase in EI by peak lactation in the 12 longitudinal studies was 1.47 MJ/day (351 kcal/day). This is considerably lower than the figure of 1.9 MJ/day (455 kcal/day) in the review by Prentice & Whitehead (1987), who estimated the change in intake during lactation from a number of cross-sectional studies. This cross-sectional analysis was however only a crude estimate of the change in intake since the majority of the baseline NPNL data did not originate from the same studies as the lactational intake data.

The measurement of habitual food intake during lactation is beset with the same potential errors which affect all studies of EI regardless of subject group. The major errors are conscious or sub-conscious underreporting of intake by the subject and/or dieting during the study period. The latter may be a particular problem although most women are aware that dieting is discouraged during lactation. The issue of measurement fatigue raised in relation to longitudinal measurements in pregnancy is unlikely to bias the current assessment of an increment of about 1.5 MJ/day, because about half of the studies measured NPNL intake after lactation

We conclude that in affluent societies it seems clear that, as in pregnancy, observed increases in EI do not match the calculated incremental costs of full lactation. These costs can be subsidised by mobilisation of body fat and/or changes in activity pattern. It would be imprudent to assume that poorly nourished women could routinely make use of either of these strategies.

Energy supply during lactation: weight changes and mobilisation of body fat

It is often assumed that lactation is associated with weight losses and that the main purpose of the extra weight and fat which is usually deposited during pregnancy is to support the energy costs of lactation. This is implicit in current recommendations for EI of lactating women which include qualifying statements according to whether fat is gained during pregnancy and/or mobilised during lactation (see Table 2). Humans stand out from many other mammals because maternal fat loss can make a very substantial contribution to the daily and overall energy costs of lactation and, since human infants grow very slowly, human milk production is low compared to other mammals of a similar body size.

Twelve longitudinal studies of weight changes in lactation, in developed and developing countries, are reviewed in this section. These studies were conducted in The Gambia (Prentice et al, 1981), USA (Brewer et al, 1989; Butte et al, 1984; Dewey et al, 1993; Manning Dalton & Allen, 1983), Sweden (Sadurskis et al, 1988), UK (Goldberg et al, 1991), The Netherlands (van Raaij et al, 1991), Mexico (Allen et al, 1992), The Philippines (Guillermo-Tuazon et al, 1992), Egypt (Kirksey et al, 1992) and Kenya (Neumann et al, 1992).

Changes in body weight. Figure 21 illustrates the changes in body weight with no distinction made by the degree of lactation (i.e. full vs partial breastfeeders). The data are presented together since, with the exception of one study (Neumann et al, 1992), there is little to suggest that there are systematic differences between developed and developing countries. However, the Gambian data have been omitted due to the over-riding influence of the season of the year.

Table 9 Longitudinal estimates of postpartum body fat changes: skinfold thicknesses



Skinfold thickness (mm)


Reference

Stage post partum

Triceps

Biceps

Subscapula

Suprailiac

Body fat
(kg or %)

Manning-Dalton et al (1983)

2 weeks

19.8

8.3

20.6

29.4



12 weeks

21.1

8.0

18.0

25.3


Butte et al (1984)

3 days

16.3

7.8

18.2

26.1

28.1%


35 days

16.9

6.9

16.8

25.7

27.6


64 days

17.0

6.9

16.4

25.2

27.3


91 days

17.3

7.3

15.7

23.1

27.2


119 days

17.2

6.8

15.1

22.2

27.0

Brewer et al (1989)a

1-2 days BF

19.7


16.4

20.8

29.60%


3 months

25.0


16.1

14.4

28.97


6 months

23.1


14.1

11.6

27.02


1-2 days FF

18.9


15.6

14.1

29.10%


3 months

21.6


14.1

12.0

27.42


6 months

19.5


12.3

11.3

26.09


1-2 days CF

23.0


14.4

18.0

30.40%


3 months

24.7


17.8

16.5

29.68


6 months

23.8


16.1

13.5

27.87

van Raaij et al (1991)b

5 weeks





19.3 kg


9 weeks





19.6


13 weeks





19.3


27 weeks





18.6


56 weeks





18.0

Guillermo-Tuazon et al (1992)b

6 weeks





12.4 kg


12 weeks





12.3


18 weeks





12.1


24 weeks





11.9


30 weeks





11.8

Dewey et al (1993)c

3 months BF

+ 1.3d






6 months

+0.1d






9 months

- 0.8d






12 months

-.1.3d






3 months FF

+ 1.5d






6 months

+ 0.6d






9 months

- 0.2d






12 months

+ 0.2d





Allen et al (1992)

0-14 days

15.7

27.6

7.6

30.6



3 months

16.8

27.8

7.7

31.5



6 months

16.5

27.7

7.6

27.1


Kirksey et al (1992)

1 months

19.9

10.7





6 months

25.3

13.8




a BF = Exclusively breast feeding; FF = exclusively formula feeding; CF = combined breast and formula feeding.
b Calculated from S Triceps, biceps, subscapula and suprailiac skinfolds.
c BF = breast-fed for ³ 12 months; FF = completely weaned by £ 3 months.
d Change in triceps (mm). Changes are calculated between measurement intervals.

Early weight losses in the studies by Butte et al (1984) and Brewer et al (1989) are substantially greater than in all the others, despite the corrections which were made for fluid losses. All the other data demonstrate that weight losses tend to occur throughout the first six months of lactation. In some instances the losses are very small and not different from those in matched groups of non-lactating post-partum women (Brewer et al, 1989; van Raaij et al, 1991). In the study by van Raaij et al, a small increase in body weight was observed. Dewey et al (1993) did observe significantly greater weight loss in full breastteeders compared to non-breastfeeders, especially to 3-6 months post partum. They argue that discrepancies between studies might be explained by a failure to adequately define true breastfeeding status.


Figure 19
Longitudinal changes in energy intake during lactation. Left-hand panel, Developed countries: Open circles, solid line, England (Whichelow, 1975); open squares, solid line, England (Black et al, 1986); closed circles, dotted line, The Netherlands (van Raaij et al, 1991); open triangles, solid line, England (Goldberg et al, 1991); open circles, dotted line, The Netherlands (van Raaij et al, 1991); closed triangles, solid line, Sweden (Sadurskis et al, 1988); closed circles, solid line. Australia (English et al, 1968); closed squares, dotted line, The Netherlands (Spaaij et al, 1994a); closed squares, solid line, Scotland (Schofield et al, 1987); open squares, dotted line, England (Schofield et al, 1987). Right-hand panel, Developing countries: Triangles, The Gambia (Prentice et al, 1981); circles, The Philippines (Guillermo-Tuazon et al, 1992); squares, Mexico (Allen et al. 1992).

Changes in body fat. Estimates of changes in body fat assessed by skinfold thicknesses are shown in Table 9. Assessments of changes by isotope dilution and whole body density are shown in Tables 10 and 11, respectively. Results are once again variable and certainly do not support the concept that fat loss is a biologically programmed part of normal lactation.

Figure 22 gives a clear indication of the reciprocal relationship that exists between a mother's incremental EI during lactation and her rate of fat loss. Mothers who have a large increase in EI tend not to lose weight. The least products regression (r = 0.550, p < 0.001) is illustrated and indicates that an energy increment of 2.70 MJ/day (645 kcal/day) is required for weight to remain constant. This is in excellent agreement with the computed costs and provides a reassuring cross validation. There seems to be no evidence that lactation is influenced by whether the energy to support it is derived from the diet or from fat stores (Prentice & Prentice, 1988).


Figure 20
Average changes in energy intake during lactation. References as for Figure 19


Figure 21
Longitudinal change in body weight in lactating women. Open circles, USA (Manning-Dalton et al, 1983); closed circles, The Gambia, dry season (Prentice et al, 1981); open squares, The Gambia, wet season (Prentice et al, 1981); closed squares, USA (Butte et al, 1984); open triangles, Sweden (Sadurskis et al, 1988); closed triangles, USA (Brewer et al, 1989); slashed squares, England (Goldberg et al, 1991); crosses, The Netherlands (van Raaij et al, 1991); (closed squares, The Philippines (Guillermo-Tuazon et al, 1992); crossed squares, USA (Dewey et al, 1993); asterisks, Mexico (Allen et al, 1992); closed diamonds, Kenya (Neumann et al, 1992); open diamonds, Egypt (Kirksey et al, 1992).

Table 10 Longitudinal estimates of changes in postpartum fat and lean body mass; isotope dilution

Reference

Baseline and stage post partum

Fat (kg)

Fat-free mass (kg)

Sadurskis et al (1988)a,b

Pre-pregnant

16.5

45.0


5-10 days

22.1

45.7


2 months

22.1

42.3


6 months

20.4

42.6

Goldberg et al (1991)c

4 weeks

17.83

41.05


8 weeks

18.28

40.60


12 weeks

18.42

40.20


3 months post weaned

15.67

41.41

a Using 18oxygen.
b Calculated from total body water and total body potassium.
c Using deuterium and 18 oxygen.

Table 11 Longitudinal estimates of changes in post-partum body fat: whole-body density

Reference

Baseline and stage post partum

Body fat (kg)

Lean body mass (kg)

Butte et al (1984)

35 d

17.2

43.7


64 d

16.5

44.0


91 d

15.8

43.8


119 d

15.6

43.2


Figure 22
Inverse relationship between incremental energy intake during lactation and rate of post-partum weight loss. (Data from AA Paul and AM Prentice, unpublished).

We conclude that a number of recent studies have indicated that significant weight losses are not obligatory during lactation, especially in well-nourished or affluent women who can support the extra energy costs incurred by increasing EI and/or decreasing physical activity. In such women the extra weight and fat may be retained and there may be further increases during lactation eventually leading to the risk of obesity. However, on average women do tend to lose about 500 g/month and it seems reasonable to build this into the recommendations in a conditional manner. We believe that the conditional nature of this offset should be stressed more strongly than in the 1985 recommendations. Since marginally-nourished women may not have been able to build up extra stores during pregnancy we recommend that the full costs of lactation should be clearly stated as the primary recommendation.

Recommendations for lactation

It is likely that the recommendations for lactation will not need to be greatly altered from the 1985 values, but the presentation could be much improved.

As for pregnancy, we propose that any effects of possible changes in activity are expressed as PAL × BMR, and that any qualitative comments that might be made are cautious and given a low profile since there is no strong consensus as to what 'usually' happens in lactation. BMR can be predicted from the Schofield equations (1985) in the same way as for non-lactating women.

We propose that the recommendation should have categories for full breastfeeders and partial breastfeeders after 3 months post partum.

With regard to weight loss and the consequent subsidizing of the costs of lactation, in our opinion fat loss is not a programmed component of lactation, as has been assumed in the past. Other behavioural and environmental factors play an important modulating role. The current assumption of approx 500 g/month seems to be a reasonable reflection of the usual pattern in well-nourished, unstressed women, but should probably not be assumed for other groups, particularly when pregnancy fat gain has been minimal. The 1985 recommendations give precedence to the assumption that lactation will be subsidised, and then state that the full cost should be met if this is not the case. We propose that this logic should be reversed and that the full costs should be clearly stated.

The overall recommendations are summarised in Table 12. If more global average figures are required we recommend the following: 2650 kJ/day (635 kcal/day) for 0-6 months with no fat loss or 2000 kJ/day (480 kcal/day) allowing for fat loss; and 2200 kJ/day (525 kcal/day) beyond 6 months for full-breastfeeders or 1200 kJ/day (285 kcal/day) for partial breastfeeders.

Table 12 Suggested figures for energy requirements during lactationa



Energy requirementc (kJ/day)

Period (month)

Milk volumeb (g/d)

Full costs

Allowing for fat lossd

All women

0-1

680

2380

1730

1-2

780

2730

2080

2-3

820

2870

2220

Full breast-feeders

3-6

820

2870

2220

6-12

650

2275

2275

12-24

600

2100

2100

Partial breast-feeders

3-6

410

1430

780

6-12

325

1140

1140

12-24

300

1050

1050

a As the text emphasises, the values are increments to be added to the maternal requirements calculated using PAL × BMR (PAL may be slightly reduced if there is evidence of lower activity during lactation in the population being considered).
b Derived from studies in Sweden (Sadurskis et al, 1988), England (Paul et al, 1988), USA (Heinig et al, 1993a,b) and the WHO Collaborative Study on Breast-Feeding (WHO, 1985). Values include a +4% adjustment to allow for insensible water losses from the baby during test-weighing.
c Assumes energy density of breast-milk to be 2.80 kJ/g and dietary milk energy conversion efficiency of 80%.
d Assumed to be approx. 500g/month up to 6 months post-partum and nothing thereafter.

Acknowledgements - The preparation of this paper was greatly assisted by written submissions from LH Allen, KG Dewey, JVGA Durnin, E Forsum, JC King, C Panter-Brick, B Schürch and Y Schutz.

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Discussion

Pregnancy

Energy requirements of pregnancy have either been estimated by summing up energy costs (tissues of the conceptus + tissue accretion in the mother + incremental maintenance costs) or inferred from energy intakes of pregnant women with successful outcome of pregnancy. Frequently the estimates obtained by the first method are substantially higher than the ones obtained by the second one. A large part of the discussion was devoted to attempts at explaining this difference.

There is a wide range in the proportion of the energy cost of pregnancy that can be spared by the mother if she substantially reduces her energy expenditure for physical activity. A considerable reduction of energy expenditure can result from relatively small changes in types and intensities of activities, which may be quite difficult to observe and record, if they all consistently go in the same direction (Durnin). In many instances this seems to actually happen and to be the main explanation for the discrepancy between energy cost estimates obtained by the two different methods. In such populations it appears reasonable to take this into account in calculations of requirements, but it should not be assumed that all pregnant women can substantially reduce their physical activity. The full cost of pregnancy should therefore remain the basis for recommendations and reductions only made where actually applicable.

Energy requirements of non-pregnant, non-lactating individuals are now generally expressed as BMR × PAL, the latter reflecting the habitual or desirable activity level, and there seems to be good agreement in the group that applying the same system to pregnant and lactating women would be a good way of accounting explicitly for differences in energy requirements for physical activity.

Earlier estimates assumed the deposition of 3 kg of fat in the mother. In their paper, Prentice et al argue for a reduction of this amount by 20%. Butte emphasized the great variability in weight gain during pregnancy and is not convinced that we have enough solid evidence to reject the earlier estimate. There is some discussion on the efficiency of fat deposition. The prevailing view seems to be that it is high since most of the fat that is deposited is dietary fat and liponeogenesis plays only a minor role (Millward & Reeds). Prentice remarked that the situation be different in countries like The Gambia, where only 16-28% of the dietary energy come from fat. If obligatory fat oxidation exceeds fat intakes and liponeogenesis becomes more important (which has not been conclusively shown yet), more energy would be needed for fat deposition. This energy would not be included in BMR, which is measured postprandially (Millward).

An intriguing phenomenon is the wide variation in the maintenance cost of pregnancy. Women with a high fat mass and BMI at conception show large increases in BMR from the beginning of pregnancy (Allen), whereas in three studies (one of them involving whole body calorimetry) the BMR of very lean women has been observed to decrease in the initial phases of pregnancy (Prentice). The physiological mechanisms underlying this variability are not clear yet, but the phenomenon raises the question whether prepregnancy BMIs or fat mass should be taken into consideration in the calculation of energy requirements. The Subcommittee on Nutritional Status and Weight Gain During Pregnancy of the National Academy of Sciences in the US (1990) recommended different weight gains during pregnancy for women with different prepregnancy BMI. A positive relationship between energy intake and weight gain during pregnancy has been observed in underweight, but not in normal-weight and overweight American women (Prentice). The idea of prescribing different energy intakes for women with different prepregnancy BMIs was considered but finally rejected because of lack of enough information on the subject.

The validity of assessments of energy intake was discussed at considerable length. Observed energy intake increments are usually considerably smaller than expected, also in women in industrialized countries, who can be assumed to eat to appetite. Since these increments tend to be smaller in longitudinal than in cross-sectional studies, measurement fatigue and underreporting were considered possible, but the evidence and the arguments presented in the discussion did not go beyond what is contained in the position paper of Prentice et al.

Increments in energy intakes and BMR throughout pregnancy are represented by an integral under a curve, and the size of this surface depends enormously on baseline values. Butte doubted if baseline data were always obtained from non-pregnant, non-lactating women.

Waterlow expressed disappointment about the fact that the report did not attempt to relate energy requirements to pregnancy outcome in terms of birthweight. Women in developing countries are usually able to maintain their body weight or even increase it through many pregnancies, whereas relatively large percentages of infants are born with a low birthweight.

Lactation

The incremental energy costs of lactation can be calculated as breast milk volume × energy density × conversion efficiency and modified by changes in maternal fat stores and activity. As in pregnancy, calculated costs of lactation are often considerably higher than the observed increments in energy intakes. Most of the difference must be attributable to a mobilization of maternal fat stores and a reduction in physical activity, but the group agreed with the authors of the position paper that, as in pregnancy, the full cost of lactation should form the basis for recommendations, i.e., loss of maternal fat and reduced physical activity of the mother should not be considered obligatory, but only taken into account where appropriate.

Milk production is remarkably robust (unaffected by BMI down to about 17 (Prentice et al, 1994) and by infection of the mother (Zavaleta et al, 1995)) and mainly driven by demand: milk donors, wet-nurses and mothers of more than one infant can increase their milk output substantially, whereas an increased energy intake does not necessarily result in a higher milk output.

The energy content of breast milk has usually been calculated by applying modified Atwater factors to proximate constituents of milk samples. This represents the metabolisable energy available to the child. The mother must supply gross energy which is about 5% higher. The fat content in the milk is highly variable and representative sampling therefore difficult. The group agrees with an estimate of about 2.8 kJ/g. Various approaches suggest that 80% is a reasonable estimate of conversion efficiency, and calculations show that changes in this assumption have relatively small effects; assuming an efficiency of 90 instead of 80% would make a difference of only about 200 kJ (Reeds).

Incremental energy intakes during lactation vary widely around an average of about 1.5 MJ. In Mexico (Allen) and The Gambia (Prentice) they are relatively high, and women gain weight during lactation; in other countries (e.g. Scotland) they are lower, probably because mothers try to lose some of the fat deposited during pregnancy.

References

Prentice AM, Goldberg GR, Prentice A (1994): Body mass index and lactation performance. Eur. J. Clin. Nutr. 48 (suppl 3), S78-S89,

Subcommittee on Nutritional Status and Weight Gain During Pregnancy (1990): Nutrition during pregnancy. Washington DC: National Academy Press.

Zavaleta N. Lanata CF, Butron B. Peerson J. Brown KH, Lönnerdal B (1995): Effect of acute infection on quantity and composition of breast milk. Am. J. Clin. Nutr. 62, 559-563.