FOOD AND AGRICULTURE ORGANIZATION OF THE UNITED NATIONSESN:FAO/WHO/UNU/
EPR/81/20

August 1981
WORLD HEALTH ORGANIZATION
THE UNITED NATIONS UNIVERSITY

Item 2.4.3 and item 3.3.3 of the Provisional Agenda

Joint FAO/WHO/UNU Expert Consultation on
Energy and Protein Requirements

Rome, 5 to 17 October 1981

ENERGY AND PROTEIN REQUIREMENTS DURING PREGNANCY.

by

J. King
University of California
Berkeley


ENERGY

Information available on the energy requirements during pregnancy is derived primarily from studies of well-nourished, healthy Western women. Preliminary evidence suggests that the metabolic adjustments in energy utilization in poorly nourished pregnant women differ markedly from the well-nourished. These differences will be discussed in greater detail later.

Two approaches have been used to estimate energy requirements during pregnancy. The factorial approach is a summation of the energy equivalents of tissue protein and fat accretion and the energy need for metabolism of the added tissue. A factor for the efficiency of conversion of dietary energy to tissue energy must be added to approximate total energy required from food. The second approach is measurement of energy expenditure using indirect calorimetry. Oxygen consumption for basal metabolism and various physical activities is measured. Total daily energy expenditures are then calculated from activity diaries. To estimate the cumulative energy cost of pregnancy, the energy equivalent of tissue gained must be added to cumulative energy expenditures.

Hytten (1), using the factorial approach, has calculated that the total energy cost of pregnancy is about 85,000 kcal (Table I). Three components comprise the total cost: the energy equivalent of the fat and protein gained in the fetus and added maternal tissues, the energy required to support metabolism of these added tissues, and an allowance for efficiency of conversion of dietary to tissue energy.

If averaged over 280 days, the cumulative energy cost of pregnancy is about 300 kcal per day. However during the first quarter there is relatively little gain of fetal or maternal tissue, and the daily additional need is thought to be only about 115 kcal per day (1). During the next two quarters extra energy is needed primarily for maternal tissue accretion which is primarily fat. This averages about 380 and 420 kcal per day in the second and third quarter, respectively. Fetal tissue gain is great in the fourth quarter, but since maternal gain is considerably reduced, the average daily cost is only about 320 kcal.

The factorial approach does not include an allowance for the extra energy which would be required for moving a heavier body during physical activity. Instead, it is frequently assumed that a reduction in activity occurs. Reduced energy expenditure may be a physiological adjustment to pregnancy in that there is a general relaxation of voluntary muscles and improved respiratory gas exchange (1). Whether these adjustments offset the cost of moving a heavier body or not is unknown.

A number of investigators have estimated total energy expenditure in pregnant women by indirect calorimetry (2–11). Total energy expenditure (TEE) is primarily comprised of three components -- basal energy expenditure (BEE), postprandial energy expenditure (PEE) and physical activity. In pregnancy a factor for tissue accretion must be added to these three.

Data compiled from several studies of basal energy expenditure (BEE) during pregnancy show an average increase of approximately 20% over non pregnant rates, with a range of 13 to 48 percent. BEE averaged 1.11 kcal per minute with a range of 1.06 to 1.17 kcal per minute in pregnant women studied; non pregnant rates ranged from 0.72 to 1.01 kcal per minute (2, 4–11). Blackburn and Calloway (7) followed changes in BEE from the 20th week of gestation to term and found consistent increases in BEE until the 36th week with no further increase thereafter.

The actual measurements of BEE are in general agreement with estimates of changes in oxygen consumption by Hytten (1). In the fourth quarter of pregnancy, the caloric equivalent of the net increase in oxygen consumption is 227 kcal per day or 0.16 kcal per minute. This is an 18 percent increase over the normal basal metabolic rate of 0.88 kcal per minute predicted for a reference non pregnant woman weighing 55 kg.

Postprandial energy expenditure (PEE) is the rise in oxygen consumption associated with eating. With intake of a meal of mixed energy sources, oxygen consumption is thought to rise about 15 percent above basal. One study of PEE showed that the net increase above basal did not differ between pregnant and non pregnant women (13). This suggests that the increased tissue synthesis occurring during pregnancy is not reflected in PEE. PEE varied from about 15 to 25 percent above basal in both the pregnant and non pregnant group.

Physical activity is the most variable component of TEE and the most difficult to assess. Measurements of oxygen consumption for various activities must be combined with 24 hour activity diaries in order to calculate total energy expenditure. The few data available from pregnant women suggest that some changes in energy expenditure for activities occur during pregnancy.

The difference in energy expenditure for quiet activities, such as lying down, sitting, and standing, is not any greater between pregnant and non pregnant women than the difference in BEE between the two groups (4, 6, 7, 14). However, the increase in energy cost for paced, weight bearing activities, such as treadmill walking, is greater than the rise in BEE. Some report that the increase and cost is proportional to the increase in body weight (4–7,9). It has also been reported (4, 6) that pregnant women tend to slow their work pace when doing self-paced tasks, i.e. stair climbing, or walking with a load (4, 6, 11). In the few studies done, a reduction in pace was not seen when light housework or window washing was performed (6, 11), suggesting that pace is altered only when the energy cost of an activity reaches a critical level. In these studies, pace was reduced when energy expenditure was greater than 2.5 times resting energy expenditure (REE).

Activity diaries from free-living Western pregnant women show that they spend about 70 to 75 percent of their time in quiet activities (7,11) and little to no time in paced weight bearing activities. Thus, the general activity pattern of these women seems to be a very sedentary one with a tendency to decrease pace when strenous work must be performed. In this population there seems to be no need to allow additional energy for the cost of moving a heavier body during pregnancy. This conclusion may not be appropriate for other population groups who must perform strenous activity throughout pregnancy.

Total energy expenditure in the last half of gestation estimated from activity diaries and oxygen consumption values averaged about 2300 kcal per day in three groups of Western women studied (6, 7, 11). Energy needs for growth are about 250 kcal per day in the third quarter of pregnancy and 70 kcal per day in the fourth (1). Thus the total energy needs for metabolism, activity and growth are 2550 and 2370 kcal per day in the third and fourth quarters, respectively. This is about 1.65 and 1.55 times BEE or 1.55 and 1.45 times REE in the last two quarters.

A safe energy allowance for the last half of gestation based on indirect calorimetry would be about 1.6 times BEE or 1.5 times REE. This would total about 2500 kcal per day for a pregnant woman with a BEE of 1.1 kcal per minute. A similar recommendation is derived using the factorial data; the addition of 300 kcal to the energy recommendation for the moderately active 55 kg reference woman (12) totals 2500 kcal.

Surveys of energy intake during pregnancy generally estimate intakes less than the predicted need. The average energy intake from several studies is about 2100 kcal per day (11). This value is probably less than the true intake because of the tendency to omit concentrated energy sources such as fat and oil when intakes are reported. The calculated energy intakes of 12 nutritionists who weighed and recorded all their food intake for three different weeks during gestation, were higher, about 2350 kcal per day (15). This value may be closer to true intakes. This intake, which was relatively constant throughout the second and third trimester, supported a mean maternal gain of 14.9 kg and a mean birthweight of 3.6 kg.

There is no evidence that energy intake varies with the stage of pregnancy (11, 15). Generally, intake increases during the first trimester and remains relatively constant thereafter with a possible slight decline near term (11,15).

These data presented on energy needs during pregnancy have been derived from healthy Western women. The situation is quite different in poorly nourished women from developing countries such as India and Guatemala.

In both of these countries the mean birthweight is about 2.9 – 3.0 kg with a maternal weight gain of 6.5 – 7.0 kg (16, 17). Thus, in those populations birthweight represents about 45% of the total maternal weight gain. In the U. S., birthweight averages about 3.3 kg, or about 25% of a total gain of 12.5 kg. A few data on triceps skinfold changes during pregnancy suggest that maternal fat stores at that site are unchanged or slightly decreased in the Indian population (18). In a group of Aberdeen women triceps skinfolds increased a small amount, and much larger increases were observed at more central sites, e.g. thigh, suprailiac and scapula (19). This suggests that the deposition of maternal fat stores may be lower in Indian women than in Aberdeen women.

If no maternal fat reserves are gained during pregnancy in marginally nourished women, this would reduce the total energy cost from 85,000 to 50,000 kcal, or the daily need from 300 to 180 kcal. Two sources for this energy exist -- maternal reserves and maternal diet.

Some maternal reserves do seem to be used by poorly nourished Indian women during pregnancy. A weight loss of about 1 kg occurs during pregnancy (20). If this loss is all fat, this would represent an availability of 9500 kcal or about 30 kcal per day. The remaining additional 150 kcal then would need to be supplied by the diet.

In populations of low income Indian and Guatemalan women the usual energy intake during pregnancy is about 1500 kcal per day and is no different from that of non pregnant women. This is about 35.5 kcal per kg for the Indian woman and about 30.5 kcal per kg for the slightly larger Guatemalan woman. Furthermore, women in these developing countries are unable to reduce their physical activity to allow more energy to be available for the needs of pregnancy. It seems, then, that very little additional energy is available from diet or maternal reserves to cover the cost of pregnancy. The only remaining explanation is that pregnant women subsisting on marginal energy intakes adapt to pregnancy differently from well nourished women, and because of this difference in adaptation they alter their energy metabolism and utilize energy more efficiently. This adaptation is not without cost to the fetus, though. When 150 kcal per day, and amount comparable to the energy deficit calculated above, were provided to poorly nourished Guatemalan women in the form of a liquid supplement, birthweight increased by 100 g (16). These data suggest a minimal energy need of 1650 kcal, or 34 kcal per kg during pregnancy for support of fetal growth. Further increases in dietary energy may be beneficial to maternal and infant health.

PROTEIN

The need for nitrogen and essential amino acids is supplied by dietary protein. To date, no studies of essential amino acid needs during pregnancy have been done. But, nitrogen needs have been predicted from factorial estimates and from balance studies.

Using factorial approach, Hytten (1) estimated that the cumulative total gain of protein in the fetus and maternal body is about 925 g. The mean daily increments of protein and nitrogen are shown in Table II. Since fetal growth occurs primarily in the last half of gestation, predicted nitrogen accretion is considerably greater the last 20 weeks than the first 20 weeks. The mean nitrogen retention during the last half of gestation is 860 mg per day; retention over all of gestation averages 530 mg N per day.

Nitrogen retention has been measured in pregnant women using the balance technique. Most of these studies were done in the last half of pregnancy, but a few observations have been made in the first half. Calloway (21) has summarized the data collected prior to 1974. Since then two additional N balance studies have been done in the metabolic unit at the University of California, Berkeley (11, 22). The results of these studies are summarized in Table III.

The N balance data suggests there is little to no difference in N accretion between the third and fourth quarters of pregnancy. The values from study II in the UCB metabolic unit are very close to the predicted rates of N accretion by Hytten (1): see Table II. The results of the other studies are slightly higher than the predicted rates. The average rate of N accretion calculated from balance data for the last half of gestation is about 1.2 g per day, or about 0.3 g greater than the predicted rate.

The predicted rate of N storage in the first half of gestation is about 0.2 g per day (1) (Table II). The balance data available suggest that the rate may be greater, about 0.7 to 1.2 g per day (Table III). N storage was similar, in the first and second trimesters, 0.7 g per day after correction for unmeasured losses, in a group of low socio-economic Indian women fed 42 g protein and 2100 kcal per day during a balance study (23). Naismith (24) has suggested a biphasic character of protein metabolism in pregnancy with protein storage occurring in early pregnancy followed by protein breakdown later. Such a pattern would modulate the effects of chronic malnutrition on fetal growth and development. Further studies of N retention and protein turnover in early and late pregnancy are needed to confirm this cycle in humans.

In conclusion, it seems that factorial estimates of N storage and N balance data predict similar rates of N storage in the last half of gestation, e.g. about 0.9 to 1.2 g N per day or 5.5 to 7.5 g protein per day. But, in the first half of gestation measured N storage is three to six times greater than the predicted gain. Until further data are available, it seems prudent to assume that the rate of N storage is constant throughout gestation and is about 1.0 g per day.

To estimate dietary N needs for support of N storage, efficiency of dietary nitrogen utilization for deposition must be considered. In all measurements of N utilization in pregnancy, the values are considerably less than that in nonpregnant healthy adults; 25 to 35 percent efficiency vs. 60 to 70 percent efficiency in nonpregnant adults (21). This low efficiency is surprising in that there appears to be enzyme changes in the liver during pregnancy which reduce its capacity to form urea, thus sparing protein for anabolic purposes (11). Dietary N might be used more efficiently at lower intakes, but this would be incompatible with maintenance of the usual rate of N accretion. For example, the mean balance of pregnant women consuming less than 10 g N per day in the last half of pregnancy was only 0.16 g per day (21).

To support a gain of 1.0 g N or 6.25 g protein per day with a 30 percent efficiency of utilization, 20 additional g protein are needed in the diet. If an additional 30 percent is added to cover individual variability, the incremental dietary protein need for pregnancy is about 25 g. Thus, a reference pregnant woman consuming a diet with a protein score of 70 should add 25 g protein to the 41 recommended for the nonpregnant state (12) bringing the total to 66 g protein per day.

It should be emphasized that in field situations both energy and protein intakes are correlated with N retention (21). Within limits, it seems that increased energy intake can compensate for lesser protein intakes. For example, regression equations predict the same rate of N storage for the following two diets, 2000 kcal with 14.0 g N as 3000 kcal with 11.2 g N. An effective ratio for N storage seems to be 7 percent protein energy. A recommendation of 66 g protein and 2500 kcal is 11 percent protein energy.

Available data show that healthy Western women generally consume more protein during pregnancy than recommended. The average protein intake of Western women eating self-selected diets is 77 g per day (11). This is 14 percent protein energy in the reported average intake of 2100 kcal. Reported intakes of women in developing countries is about 40 g protein per day (16, 17), or about 11 percent protein energy in the usual 1500 kcal intake. This is comparable to the recommended protein energy concentration, but if total energy is marginal, protein may be less available for tissue synthesis. Oldham and Sheft (25) have shown that at least 36 kcal per kg are required during pregnancy for support of N retention.

TABLE I

Total energy cost of pregnancy calculated from the energy equivalents of tissue gained and the energy required to maintain that tissue.a)

 gkcal equivalenttotal kcal
Protein9255.6 kcal/g5,180
Fat3,8259.5 kcal/g36,337
Oxygen Consumption10,293 ml3.47 kcal/ml35,717
Total Net Energy  77,234
Metabolizable Energy
(Total + 10%)
  84,957

a) Adapted from reference 1.



TABLE II

Estimated Protein and Nitrogen
Retention during Pregnancy Assuming
that the Fetus weighs 3.30 kg at Term.a)

Stage of GestationProtein
g/day
Nitrogenb)
mg/day
First quarter0.64100
Second quarter1.84295
Third quarter4.76760
Fourth quarter6.10975

a) Adapted from reference 1.

b) Calculated form protein value assuming protein is 16 percent nitrogen.



TABLE III

Nitrogen Retention during Pregnancy
as measured in Balance
Studied, g per day.

Stage of GestationSummary ofa
Data Collected
Prior to 1974
UCB Metabolic Unit
Study IbStudy IIc
First quarter1.2d(1)e----
Second quarter0.7(39)----
Third quarter1.25(119)1.45d(12)0.7d(20)
Fourth quarter1.35(184)1.49(20)0.8(16)

a) Adapted from Calloway (21); primarily studies of women living at homeand eating their usual diet.

b) Adapted from Appel (11). An egg albumin based formula diet providing0.8 g protein/kg prepregnant weight plus 30 g for pregnancy was fed.

c) Adapted from Swanson (22). A blenderized natural food diet made primarily from meat or vegetable sources was fed. The two diets contained either 99 or 92 g protein/day; no adjustments in protein intake were made for body size.

d) After correction for unmeasured losses; 0.4 g N was allowed for integumental hair, nails, vaginal secretions, tooth brushings, exhaled ammonia,excreta on tissues and collecting devices, and plate waste.

e) Number of balances.

LITERATURE CITED

  1. Hytten, F.E. Nutrition. In: Clinical Physiology in Obstetrics. Edited by F. Hytten and G. Chamberlain. Oxford: Blackwell Scientific Publications. 1980.

  2. Sandiford, J. and T. Wheeler. The basal metabolism before, during and after pregnancy. J. Biol. Chem. 62:329. 1924–25.

  3. Rowe, A.W. and W.C. Boyd. The metabolism in pregnancy. 9. The foetal influence on the basal rate. J. Nutr. 5:551. 1932.

  4. Banerjee, B., K.S. Khew, and N. Saha. A comparative study of energy expenditure in some common daily activities of non-pregnant and pregnant Chinese, Malay and Indian women. Br. J. Obstet. and Gynecol. 78:113. 1971.

  5. Emerson, K., B.N. Saxena, and E.L. Poindexter. Caloric cost of normal pregnancy. Obstet. and Gynecol. 40:786. 1972.

  6. Blackburn, M.L. and D.H. Calloway. Energy expenditure of pregnant adolescents. J. Am. Dietet. Assoc. 65:24. 1974.

  7. Blackburn, M.L. and D.H. Calloway. Basal metabolic rate and work energy expenditure of mature, pregnant women. J. Am. Dietet. Assoc. 69:24. 1976.

  8. Juen, U., Y. Kagawa, S. Kagawa, K. Hasegawa, K. Koike and S. Toda. Studies on pregnancy and after delivery 1. On the basal metabolism in the normal pregnancy. J. Jap. Soc. Food Nutrition. 23:513. 1970.

  9. Knuttgen, H.G. and K. Emerson, Jr. Physiological response to pregnancy at rest and during exercise. J. Applied Physiol. 36:549 1974.

  10. Blackburn, M.W. and D.H. Calloway. Energy expenditure and consumption of mature, pregnant and lactating women. J. Am. Dietet. Assoc. 69:29. 1976.

  11. Appel, J.A. Protein and energy utilization in pregnant and non-pregnant women. Doctoral dissertation. Univ. of California, Berkeley. 1980.

  12. Joint FAO/WHO Ad Hoc Expert Committee. Energy and Protein Requirements. Geneva: World Health Org. techn. Rep. Ser. No. 522. 1973.

  13. Schultz, Y., J.C. King and S. Margen. Postprandial and basal energy expenditures (PEE & BEE) in pregnant (P) and non pregnant (NP) women. XII International Congress of Nutrition. 1981. (Abstract).

  14. Seitchik, J. Body composition and energy expenditure during rest and work in pregnancy. Am. J. Obstet. and Gynecol. 97:701. 1967.

  15. King, J.C., J. Alberts, and A.M. Kodama. Nitrogen and potassium retention in healthy pregnant women. Fed. Proc. 35:597. 1976. (Abstract).

  16. Lechtig, A. J.P. Habicht, H. Delgado, R.E. Klein, C. Yarbrough and R. Martorell. Effect of food supplementation during pregnancy on birthweight. Pediatrics. 56:508. 1975.

  17. Rajalakshmi, R. Reproductive performance of poor Indian women on a low plane of nutrition. Trop. Geogr. Med. 23:117. 1971.

  18. Anom. Urban-rural differences in maternal nutritional status during pregnancy. Annual Report of the National Institute of Nutrition. Hyderabad: Indian Council of Med. Res. 1980. p. 64–65.

  19. Taggart, N.R., R.M. Holliday, W.Z. Billewicz, F.E. Hytten and A.M. Thompson. Changes in skinfolds during pregnancy. Br. J. Nutr. 21:439. 1967.

  20. Anom. Longitudinal studies of weight changes in pregnancy in undernourished women. Annual report of the Nutrition Research Laboratories. Hyderbad: Indian Council of Med. Research. 1967. p. 66–67.

  21. Calloway, D.H. Nitrogen balance during pregnancy. In: Nutrition and Fetal Development. Vol. 2. Edited by M. Winick. New York: John Wiley and Sons. 1974.

  22. Swanson, C. The effect of dietary zinc sources on zinc utilization in pregnant and nonpregnant women. Doctoral dissertation. Univ. of California, Berkeley. 1980.

  23. Rao, C.N. and B.S.N. Ras. Nitrogen balance in pregnancy and lactation in women whose protein intake is marginal. Indian J. Med. Res. 62:1619. 1974.

  24. Naismith, D. J. Maternal nutrition and the outcome of pregnancy - a critical appraisal. Proc. Nutr. Soc. 39:1. 1980.

  25. Oldham, H. and B.B. Sheft. Effect of caloric intake on nitrogen utilization during pregnancy. J. Am. Dietet. Assoc. 27:847. 1951.



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