6. ENERGY REQUIREMENTS OF PREGNANCY

Dietary intake during pregnancy must provide the energy that will ensure the full-term delivery of a healthy newborn baby of adequate size and appropriate body composition by a woman whose weight, body composition and PAL are consistent with long-term good health and well-being. The ideal situation is for a woman to enter pregnancy at a normal weight and with good nutritional status. Therefore, the energy requirements of pregnancy are those needed for adequate maternal gain to ensure the growth of the foetus, placenta and associated maternal tissues, and to provide for the increased metabolic demands of pregnancy, in addition to the energy needed to maintain adequate maternal weight, body composition and physical activity throughout the gestational period, as well as for sufficient energy stores to assist in proper lactation after delivery. Special considerations must be made for women who are under- or overweight when they enter pregnancy.

This consultation reviewed recent information on the association of maternal weight gain and body composition with the newborn birth weight, on the influence of birth weight on infant mortality, and on the associated metabolic demands of pregnancy (WHO, 1995a; Kelly et al., 1996; Butte and King, 2002), in order to perform factorial calculations of the extra energy required during this period. It was acknowledged that estimates of energy requirements and recommendations for energy intake of pregnant women should be population-specific, because of differences in body size, lifestyle and underlying nutritional status. Well-nourished women raised in affluent or economically developed societies may have different energy needs in pregnancy than women from low-income developing societies; pregnancy energy requirements of stunted or undernourished women may differ from those of overweight and obese women; and physical activity patterns may change during pregnancy to an extent that is determined by socio-economic and cultural factors. Even within a particular society, high variability is seen in the rates of gestational weight gain and energy expenditure of pregnant women, and therefore in their energy requirements.

6.1 Gestational weight gain and optimal pregnancy outcome

The WHO Collaborative Study on Maternal Anthropometry and Pregnancy Outcomes (WHO, 1995a; Kelly et al., 1996) reviewed information on 110 000 births from 20 countries to determine anthropometric indicators associated with poor foetal outcomes, such as low birth weight (LBW), intrauterine growth retardation (IUGR) and pre-term birth, and with poor maternal outcomes, such as pre-eclampsia, eclampsia, need for assisted delivery, and postpartum haemorrhage. Attained maternal weight (pre-pregnancy weight plus weight gain) was the most significant predictor of LBW and IUGR (with odds ratios of 2.5 and 3.1, respectively). Low pre-pregnancy weight and BMI, and weight gain between 20 and 28 weeks of gestation were moderate predictors of pre-term delivery (odds ratios of 1.3 and 1.4, respectively), and low maternal height (e.g. 146 compared with 160 cm) was a moderate predictor of caesarean delivery (odds ratio: 1.6) (Merchant, Villar and Kestler, 2001).

Women with short stature, especially in developing countries with inadequate health care systems and high prevalence of impaired growth during childhood, are also at high risk of LBW and pre-term delivery, and of obstetric complications during labour and delivery (WHO, 1995a; Martorell et al., 1981). A study of healthy women with uncomplicated pregnancies in the United States showed a positive association between maternal height and birth weight among white, black and Asian women, but not Hispanic women (Picket, Abrams and Selvin, 2000).

6.1.1 Desirable birth weight and gestational weight gain

Weight gain during pregnancy comprises the products of conception (foetus, placenta, amniotic fluid), the growth of various maternal tissues (uterus, breasts) and the increase in blood, extracellular fluid and maternal fat stores. The desirable amount of weight to be gained is that which is associated with optimal outcome for the mother, in terms of preventing maternal mortality and complications of pregnancy, labour and delivery, and allowing adequate postpartum body weight and lactation performance; and with optimal outcome for the infant, in terms of allowing adequate foetal growth and maturation, and in the prevention of gestational and perinatal morbidity and mortality. The WHO Collaborative Study on Maternal Anthropometry and Pregnancy Outcomes showed that birth weights between 3.1 and 3.6 kg, with a mean of 3.3 kg, were associated with the optimal ratio of good foetal and maternal outcomes (WHO, 1995a; Kelly et al., 1996). The range of maternal gestational weight gains associated with such birth weights was between 10 and 14 kg, with a mean of 12 kg. This is in agreement with earlier estimates that healthy women in developing countries, who eat in accordance with appetite, gain 10 to 12 kg (Institute of Medicine, 1992). An analysis of gestational weight gains associated with optimal outcomes and full-term delivery of 3- to 4-kg infants in the United States gave a similar although somewhat higher range (11.5 to 16.0 kg) for women with pre-pregnancy BMI between 19.8 and 26.0 (Institute of Medicine/Food and Nutrition Board, 1990; Abrams, Altman and Pickett, 2000).

This consultation endorsed the WHO recommendation that healthy, well-nourished women should gain 10 to 14 kg during pregnancy, with an average of 12 kg, in order to increase the probability of delivering full-term infants with an average birth weight of 3.3 kg, and to reduce the risk of foetal and maternal complications.

6.2 Determinants of the energy cost of pregnancy

The energy cost of pregnancy is determined by the energy needed for maternal gestational weight gain, which is associated with protein and fat accretion in maternal, foetal and placental tissues, and by the increase in energy expenditure associated with basal metabolism and physical activity. It was estimated by previous FAO/WHO/UNU expert committees and consultations (FAO/WHO, 1973; WHO, 1985) through factorial calculations based on a theoretical model that assumed an average gestational weight gain of 12.5 kg, an average infant birth weight of 3.4 kg, cumulative deposition of 925 g protein and 3 825 g fat, an efficiency of energy utilization of 90 percent, and a cumulative increment of 150 MJ in BMR (Hytten, 1980; Hytten and Chamberlain, 1991). Since then, several longitudinal studies in developed and developing countries have allowed for the revision of these theoretical estimates.

6.2.1 Protein and fat deposition during pregnancy

Protein is deposited predominantly in the foetus (42 percent), but also in the uterus (17 percent), blood (14 percent), placenta (10 percent) and breasts (8 percent) (Hytten, 1980; Hytten and Chamberlain, 1991). Total protein deposition has been estimated indirectly from calculations of total body potassium accretion, measured by whole body counting in a number of studies of pregnant women (Butte and King, 2002). Based on results of the most reliable longitudinal studies, which involved 93 women in Sweden (Forsum, Sadurskis and Wager, 1988), the United Kingdom (Pipe et al., 1979) and the United States (King, Calloway and Margen, 1973; Butte et al., 2003), and assuming a potassium to nitrogen (K:N) ratio of 2.15 meq K/g N in foetal tissues, protein deposition was estimated at 686 g, in association with a gestational weight gain of 13.8 kg (Butte and King, 2002). The corresponding protein gain associated with the mean weight gain of 12 kg (range 10 to 14 kg) observed in the WHO collaborative study would be 597 g (range 497 to 696 g).

Cumulative fat deposition in foetal and maternal tissues contributes substantially to the overall energy cost of pregnancy. Therefore, methodological errors in the estimation of fat accretion can affect significantly the calculation of energy requirements. Calculations based on skin-fold measurements lack the precision for an accurate estimate of changes in fat mass during pregnancy, because fat accumulation is not distributed evenly in all parts of the body. Two-component body composition models based on measurement of total body water, body density or total body potassium are acceptable only if they include appropriate corrections to account for pregnancy-related changes in the hydration, density and potassium content of fat-free mass (Butte and King, 2002). Three- and four-component models where the hydration or density of fat-free mass is measured are acceptable to calculate body fat at various stages of pregnancy.

Fat accretion was calculated from the results of 11 longitudinal studies that used three- and four-component body composition models, or two-component models with corrected constants, in 273 well-nourished pregnant women from the Netherlands (van Raaij et al., 1988; Spaaij, 1993; de Groot et al., 1994), Sweden (Forsum, Sadurskis and Wager, 1988; Sohlström and Forsum, 1997), the United Kingdom (Pipe et al., 1979; Goldberg et al., 1993) and the United States (Butte et al., 2003; Lederman et al., 1997; Lindsay et al., 1997; Kopp-Hoolihan et al., 1999a). Mean fat accretion measured up to 36 weeks of gestation was 3.7 kg, associated with a mean weight gain of 11.9 kg. Extrapolating the calculations to 40 weeks of gestation increased mean fat accretion to 4.3 kg, associated with a mean weight gain of 13.8 kg (Butte and King, 2002). The fat gain associated with the mean weight gain of 12 kg (range 10 to 14 kg) observed in the WHO collaborative study would be 3.7 kg (range 3.1 to 4.4 kg).

Rates of fat accretion during the first, second and third trimesters of pregnancy were available in a subset of the studies mentioned (Forsum, Sadurskis and Wager, 1988; Pipe et al., 1979; Butte et al., 2003; de Groot et al., 1994; Goldberg et al., 1993; Kopp-Hoolihan et al., 1999a). These were, on average, 8 g/day in the first trimester, and 26 g/day in the second trimester. Results varied markedly in the third trimester, from -7 to 23 g/day (average: 8 g/day), but if the three studies with very low mean values (-7.0, -1.4 and 4.8 g/day) are excluded from calculations, the average accretion rate would be 18 g fat/day in the third trimester.

6.2.2 Basal metabolism in pregnancy

Basal metabolism increases in pregnancy as a result of accelerated tissue synthesis, increased active tissue mass, and increased cardiovascular and respiratory work. Several studies have measured basal or resting metabolic rate at several stages of pregnancy. As energy requirements should be based on healthy populations with favourable pregnancy outcomes, this consultation only considered the results of studies that involved healthy, well-nourished groups of women with adequate weight gains during pregnancy, who gave birth to infants with adequate weights (Table 6.1) (Forsum, Sadurskis and Wager, 1988; de Groot et al., 1994; Goldberg et al., 1993; Durnin et al., 1987; van Raaij et al., 1987; Spaaij et al., 1994; Piers et al., 1995; Muthayya, 1998; Kopp-Hoolihan et al., 1999b; Cikrikci, Gokbel and Bediz, 1999).

As Table 6.1 shows, the cumulative increment in BMR calculated in relation to pre-pregnancy values, or to early pregnancy values when pre-pregnancy BMR was not available, ranged from 124 to 200 MJ, with an average increase of 154 MJ for the entire gestational period. The average increases in BMR over pre-pregnancy values were in the order of 5, 10 and 25 percent for the first, second and third trimesters, respectively. The coefficient of variability of the cumulative increase in BMR was 16 percent between studies, but the variability between women in each study was higher, with a cumulative variability of 45 to 70 percent in many cases. This demonstrates once again that the application of mean population requirements to specific individuals may lead to large errors. The variation in BMR during pregnancy, which is further illustrated by a striking reduction well into the third trimester of pregnancy found among undernourished Gambian women (Lawrence et al., 1987), a depression in BMR up to 24 weeks of gestation reported in groups of well-nourished United Kingdom (Prentice et al., 1989) and Netherlands (Spaaij, 1993) women, and a cumulative reduction or low increase in BMR during pregnancy among some United States women (Kopp-Hoolihan et al., 1999b).

Cumulative increases in BMR are significantly correlated with gestational weight gain (r = 0.79; p < 0.001) and pre-pregnancy percentage fat mass (r = 0.72; p < 0.001) (Prentice et al., 1996). Hence, the cumulative increase of 154 MJ associated with an average gestational weight gain of 12.5 kg (Table 6.1) would correspond to 148 MJ for a weight gain of 12 kg. These values are remarkably close to the 150 MJ estimated from changes in oxygen consumption of individual organs (Hytten, 1980), which was used by previous expert consultations (FAO/WHO, 1973; WHO, 1985).

6.2.3 Total energy expenditure during pregnancy

A review of 122 studies on practices related to work and pregnancy indicated that in most societies women were expected to continue with partial or full household and other duties throughout most of pregnancy (Institute of Medicine, 1992). Similarly, a review and summary of time-motion studies in Scotland, the Netherlands, Thailand, the Philippines, the Gambia and Nepal did not find conclusive evidence that women engaged in less activity during pregnancy and thus reduced their energy expenditure (Prentice et al., 1996). But these studies did not give information about changes in the intensity of the effort associated with habitual tasks. However, there was a suggestion of increased efficiency in energy utilization for physical activity during pregnancy, as the energy cost of weight-bearing activities remained fairly constant during the first two trimesters of pregnancy, even though body weight had increased by 5 to 8 kg by the end of the second trimester (Prentice et al., 1996).

Longitudinal measurements with DLW in free-living, well-nourished women in Sweden (Forsum et al., 1992), the United Kingdom (Goldberg et al., 1993 and 1991) and the United States (Butte et al., 2003; Kopp-Hoolihan et al., 1999b) showed a mean increase of 16.5 percent in TEE by the third trimester of pregnancy, compared with non-pregnant values (Table 6.2). Some of these studies provided information at each trimester of pregnancy and in the non-pregnant state, suggesting that TEE increased by about 1, 6 and 17 percent in the first, second and third trimesters of pregnancy, respectively. This was proportional to recorded increments in weight gain of 2, 8 and 18 percent during the same periods ((Butte and King, 2002). The relationship between TEE and weight gain is reflected in the lack of difference between non-pregnant and pregnant women when TEE is expressed per kilogram of body weight (Table 6.2). The estimated increments in TEE were 100, 400 and 1 500 kJ/day (25, 95 and 360 kcal/day) in the first, second and third trimesters of pregnancy, respectively, in association with an average weight gain of 13.8 kg (Butte and King, 2002). For an average gain of 12 kg, the corresponding values would be 85, 350 and 1 300 kJ/day (20, 85 and 310 kcal/day).

Because of the larger increment in BMR, especially in the second and third trimesters of pregnancy (Table 6.1), PAL declined from 1.74 prior to pregnancy to 1.60 in late gestation (Table 6.2). Compared with non-pregnant values, total energy expenditure to activity (activity energy expenditure [AEE]) near the end of gestation ranged from a decrease of 22 percent to an increase of 17 percent, but on average did not differ significantly between non-pregnant women and women in the third trimester of pregnancy (3 percent ± 15 percent, Table 6.2). However, when expressed per unit of body weight, there was a tendency towards lower AEE/kg/day in the last trimester of pregnancy.

Cross-sectional studies with DLW, HRM or time-motion techniques in Colombia (Dufour, Reina and Spurr, 1999), Nepal (Panter-Brick, 1993), and two (Heini et al., 1991; Lawrence and Whitehead, 1988) of three (including Singh et al., 1989) studies in the Gambia, showed a slight decrease in TEE, ranging from 1 to 7 percent, and larger reductions, from 10 to 38 percent, in AEE by the third trimester of pregnancy, relative to non-pregnant controls (Butte and King, 2002). This was consistent with observations that many women perform less arduous tasks as they approach the end of pregnancy.

6.3 Calculation of energy requirements for pregnancy

The extra amount of energy required during pregnancy was calculated in association with a mean gestational weight gain of 12 kg by two factorial approaches, using either the cumulative increment in BMR during pregnancy (section 6.2.2) or the cumulative increment in TEE (section 6.2.3), plus the energy deposited as protein and fat (section 6.2.1). In the calculations using the increment in BMR, it was assumed that the efficiency in energy utilization to synthesize protein and fat was 90 percent. Adjustments for efficiency of energy utilization were not necessary in the calculations that used the increment in TEE, as TEE measured with DLW includes the energy cost of synthesis. As Table 6.3 shows, the estimates of the additional energy required during pregnancy were very similar using either BMR or TEE for the calculations: 323 MJ (77 100 kcal) and 320 MJ (76 500 kcal), respectively. These values, which were based on experimental data, differ by only 4 percent from the theoretical estimate of 335 MJ (80 000 kcal) made by the 1981 FAO/WHO/UNU expert consultation (WHO, 1985).

The energy cost of pregnancy is not distributed equally throughout the gestational period. The deposition of protein occurs primarily in the second (20 percent) and third trimesters (80 percent). Assuming that the rate of fat deposition follows the same pattern as the rate of gestational weight gain, 11, 47 and 42 percent of fat is deposited in the first, second and third trimesters, respectively (Institute of Medicine/Food and Nutrition Board, 1990). The increments in BMR in these trimesters are about 5, 10 and 25 percent, respectively (section 6.2.2 and Table 6.2), whereas the increase in TEE for women gaining 12 kg in pregnancy was estimated at about 85, 350 kcal/day and 1 300 kJ/day per trimester (section 6.2.3).

TABLE 6.1
Cumulative increase in basal metabolic rate of well-nourished women during pregnancy

^a Weight gain was extrapolated to 40 weeks of gestation, assuming that the average weight gain during the first ten to 12 weeks of pregnancy is 0.65 kg, and that weight gain increases in the last four to eight weeks by 0.40 kg/week (Hytten and Chamberlain, 1991).
^b Calculated as cumulative increase throughout pregnancy in relation to pre-pregnancy or early pregnancy values of BMR.
^c Non-weighted averages and standard deviations of the mean results in the studies shown in this table.

TABLE 6.2
Total energy expenditure measured with DLW in well-nourished non-pregnant and pregnant women

^a Preg = pregnant.
^b NP = non-pregnant.
^c Based on estimated mean body weight.
^d Standard deviation of mean.

TABLE 6.3
Additional energy cost of pregnancy in women with an average gestational weight gain of 12 kg^*

* Calculated as suggested by Butte and King (2002). Weight gain and tissue deposition in first trimester computed from last menstrual period (i.e. an interval of 79 days). Second and third trimesters computed as 280/3 = 93 days each.
^a Protein and fat deposition estimated from longitudinal studies of body composition during pregnancy, and an energy value of 23.6 kJ (5.65 kcal)/g protein deposited, and 38.7 kJ (9.25 kcal)/g fat deposited.
^b Efficiency of food energy utilization for protein and fat deposition taken as 0.90 (Hytten, 1990).
^c Efficiency of energy utilization not included in this calculation, as the energy cost of synthesis is included in the measurement of TEE by DLW.

Based on these considerations and averaging the two factorial calculations shown in Table 6.3, the extra energy cost of pregnancy is 321 MJ (77 000 kcal) divided into approximately 0.35 MJ/day, 1.2 MJ/day and 2.0 MJ/day (85 kcal/day, 285 kcal/day and 475 kcal/day) during the first, second and third trimesters, respectively. There are many societies with a high proportion of non-obese women who do not seek prenatal advice before the second or third month of pregnancy. Under these circumstances a practical option to achieve the total additional intake of 321 MJ (77 000 kcal) during pregnancy is to add the extra 0.35 MJ/day required in the first trimester to the 1.2 MJ/day required in the second trimester. Rounding numbers for ease of calculation, this consultation recommends that in such societies pregnant women increase their food intake by 1.5 MJ/day (360 kcal/day) in the second trimester, and by 2.0 MJ/day (475 kcal/day) in the third.

The preceding joint FAO/WHO/UNU expert consultation suggested that the additional energy allowance could be lowered in cases where women reduce their activity level during pregnancy. When such a reduction occurred among the women who participated in the studies listed in Table 6.2, it was built into the 24-hour TEE used to calculate the energy cost of pregnancy in Table 6.3. On the other hand, not all women have the option to reduce physical activity during pregnancy. In particularly, low-income women from developing countries must often continue a strenuous work pattern until shortly before delivery. Furthermore, women who are sedentary prior to pregnancy have little flexibility to reduce their level of physical activity. Consequently, this consultation does not recommend a reduction in the additional energy allowance for pregnancy.

6.4 Special considerations for malnourished, obese and adolescent pregnant women

Undernutrition, whether manifested as underweight or as stunting, and obesity increase the risk of poor maternal and foetal outcomes. Ideally, women should begin pregnancy at a healthy weight, defined as a BMI between 18.5 and 24.9 (WHO, 1995a; March of Dimes, 2002). Adolescent girls who are pregnant must fulfil the dietary requirements imposed by growth associated with their age, in addition to the extra demands of pregnancy.

6.4.1 Pregnancy and undernutrition

A large number of women in many parts of the world enter pregnancy at suboptimal weight and/or height. An analysis of studies in 20 countries (Kelly et al., 1996) showed that in ten countries many women had pre-pregnancy weights of < 50 kg and heights of < 150 cm. These cut-off points were associated with increased risks of maternal complications. In addition, weight below 45 kg or height below 148 cm were associated with poor foetal outcomes. The linear relationship between gestational weight gain and birth weight is influenced by maternal pre-pregnancy BMI, such that women with a BMI < 18.5 must gain more weight than those with a normal BMI in order to have babies with adequate birth weight. It is then particularly important that underweight women increase their energy intake to gain the prescribed 10 to 14 kg during pregnancy, depending on their height (e.g. taller women should strive for a weight gain of 14 kg). Gestational weight gains as high as 18 kg have been suggested for undernourished women (Institute of Medicine/Food and Nutrition Board, 1992).

The association of short stature with increased risk of either delivering a low birth weight infant or requiring special assistance during delivery owing to cephalo-pelvic disproportion (Merchant, Villar and Kestler, 2001) indicates the importance for such women to have adequate prenatal attention and access to appropriate care during labour and delivery. This also reinforces the recommendations for good nutrition and measures to prevent repeated infections during childhood, which may result in stunting and in pregnancy-related problems at a later age.

6.4.2 Pregnancy and obesity

Maternal obesity is also associated with a higher risk of maternal and foetal complications. As for undernutrition, the relative risks of neural tube defects, congenital malformations and pre-term delivery are higher in overweight and obese women (March of Dimes, 2002). Incidences of hypertension, gestational diabetes and the need for caesarean section operations are also higher than in women with normal weight.

Women with a pre-pregnancy BMI > 25 tend to have babies with high birth weights, even when the women have relatively low gestational weight gains (Institute of Medicine/Food and Nutrition Board, 1992; Shapiro, Sutija and Bush, 2000). As this may lead to problems during delivery, it is likely that such women will be better off gaining weight at, or somewhat below, the lower limit of the 10 to 14 kg range recommended for women with normal BMI. It has been suggested that weight gain should be as low as 7 kg for women who enter pregnancy with BMI > 26 (Institute of Medicine/Food and Nutrition Board, 1992).

6.4.3 Pregnancy in adolescence

It is important to satisfy the energy needs of adolescence, when as much as 20 percent of total growth in stature can occur (WHO, 1995b). These needs increase during gestation and must be satisfied by appropriate dietary intakes to satisfy the requirements of both adolescence and pregnancy, in order to allow adequate maternal and foetal growth.

Compared with older women, those under 18 years of age have an increased risk of pre-term delivery, giving birth to infants with low birth weight or small size for gestational age, and requiring special obstetrical assistance (Kumbi and Isehak, 1999; Larsson and Svanberg, 1983; Bwibo, 1985; Gortzak-Uzan et al., 2001). The risks increase with decreasing age (Bwibo, 1985; Bhalerao et al., 1990). Owing to the high incidence of complications associated with an immature body and small size, it is essential that, in addition to a suitable diet, adolescent pregnant girls receive adequate prenatal care and have access to appropriate medical facilities during labour and delivery.

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