Nutrient Metabolism and Physical Activity

National Research Council (US) Subcommittee on Nutrition and Diarrheal Diseases Control; National Research Council (US) Subcommittee on Diet, Physical Activity, and Pregnancy Outcome

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National Research Council (US) Subcommittee on Nutrition and Diarrheal Diseases Control; National Research Council (US) Subcommittee on Diet, Physical Activity, and Pregnancy Outcome. Nutrition Issues in Developing Countries: Part I: Diarrheal Diseases: Part II: Diet and Activity During Pregnancy and Lactation. Washington (DC): National Academies Press (US); 1992.

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Nutrition Issues in Developing Countries: Part I: Diarrheal Diseases: Part II: Diet and Activity During Pregnancy and Lactation.

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4Nutrient Metabolism and Physical Activity

Energy

Energy is the primary dietary requirement. If the overall intake of energy is inadequate, dietary protein, vitamins, and minerals will not be used effectively for their various metabolic functions. Durnin (1987) estimated that the energy cost of pregnancy is about 60,000 kcal among well-fed women. Based on the composition of the average weight gain and the cost of its accretion and maintenance, Hytten (1980b) estimated that the energy requirement for pregnant women who have an adequate prepregnancy nutritional status totals 85,000 kcal, or 300 additional kcal/day if the need is distributed equally over the 280 days of gestation. Of the 85,000 kcal, about 41,000 kcal are deposited as the accretion of fat and lean tissue, and about 36,000 kcal are required for the increased metabolism rate (Table 4-1). An additional 8,000 kcal are needed to convert dietary energy to metabolizable energy. It is thought that the energy demand is distributed equally throughout the last 10 weeks of the pregnancy. Deposition of about 3.5 kg of fat in the maternal compartment accounts for two-thirds of the total energy need during the second and third quarters of pregnancy. Fetal growth needs are maximal in the fourth quarter.

TABLE 4-1

Cumulative Energy Cost of Pregnancy Computed from the Energy Equivalents of Protein and Fat Increments and the Energy Cost of Maintaining the Fetus and Added Maternal Tissues.

Resting or Basal Energy Requirements

Many investigators have attempted to confirm the estimated energy requirement for pregnancy by measuring the two major components of energy expenditure: resting metabolism and energy expenditure during periods of activities. These two aspects may account for 90 percent or more of the total energy expenditure.

Measurements of energy expenditure for metabolism (i.e., basal (BMR) or resting (RMR) metabolic rate) from several groups of pregnant women are given in Table 4-2 (Blackburn and Calloway, 1976; Durnin et al., 1985; Forsum et al., 1985; Lawrence et al., 1984, Nagy and King, 1983). For comparison, the estimated RMR during pregnancy and its total energy cost (Hytten, 1980a) are also presented. The additional amount of energy used for RMR should be comparable with the estimated need for metabolism, that is, 36,000 kcal/pregnancy (Hytten, 1980a). Resting energy metabolism increased in all the groups of women studied, but the incremental increase varied greatly among the groups. The biggest net change in resting metabolism was seen in Swedish women (46,500 kcal), whereas the unsupplemented women in The Gambia (see Chapter 3) had the lowest change (1,000 kcal).

TABLE 4-2

Energy Expenditures of Pregnant Women at Rest.

Studies from The Gambia suggest that maternal nutritional status influences the level of change in resting metabolism during gestation. The unsupplemented women, who consumed only 1,500 kcal/day, had lower RMRs in the second and third trimesters than did the women who received supplements and consumed about 1,950 kcal/day (Lawrence et al., 1984; Prentice et al., 1983). The supplemented women required an additional 13,000 kcal for resting metabolism; only 1,000 kcal were required by the unsupplemented women (Table 4-1).

Conventional formulas make no allowance for the increased energy costs required to move a heavier body because it is assumed that pregnant women compensate for the increased energy need for physical activity by becoming more sedentary or by performing tasks in a more relaxed or energy-efficient manner (Banerjee et al., 1971; Emerson et al., 1972, Hytten, 1980a).

However, physical activity and exercise recently have become more popular among women living in industrialized societies, and the effects of such programs on the energy requirements during gestation depend on the frequency, intensity, and duration of exercise. Although studies of the energy expenditure of pregnant women who regularly take part in recreational activities have not been done, one group of investigators reported that the energy intakes of women who jog throughout their pregnancies are similar to those reported by sedentary pregnant women studied previously (Slavin et al., 1985). There is some evidence that physical activity improves the efficiency of energy use in nonpregnant women (King and Butterfield, 1986). If this is also true in pregnant women, the net energy cost for physical activity among fit pregnant women may be less than expected.

Energy Requirements for Activity

The amount of energy expended during physical activity fluctuates with the intensity, duration, and type of exercise, as well as body weight. Tables are available for estimating energy expenditure for a variety of activities based on the individual's body weight. Because of weight gain during pregnancy, the energy required for weightbearing activity should increase gradually with advancing gestation. The energy expenditure for nonweightbearing activity may also be higher in pregnant women as a result of the increased basal metabolic rate, especially during the second half of pregnancy. The efficiency of a person's movements also influences the total energy expenditure for activity. Runners who have smooth, comfortable gaits expend fewer calories than those who struggle all the way. It has been stated that pregnant women move in a more economical manner (Hytten, 1980a). If movements become more efficient during pregnancy, the energy cost for activity during pregnancy may be lower than that in the nonpregnant state. Separate tables for physically active pregnant women may be useful to adjust the energy expenditure for changes in basal metabolism and efficiency of movements (Table 4-3).

TABLE 4-3

Energy Cost of Activities During Pregnancy.

The amount of energy required for quiet or light activities that do not involve body movement is reflected in the change in resting metabolism. The energy requirements for activities involving body movement reflect the amount of weight gain as well as the change in resting metabolism.

Comparisons of the energy expenditures for common household tasks in pregnant and nonpregnant women (Banerjee et al., 1971) showed that pregnant women expend more total energy for a given task, but the net increase in energy expenditure above the resting expenditure is lower in pregnant than in nonpregnant women. This suggests that the pregnant women performed the tasks in a more relaxed or economical fashion, that is, they reduced their work intensity. A similar decrease in work intensity was seen in the second and third trimesters of pregnancy among women in The Gambia (Lawrence et al., 1985). Energy expenditures above the resting metabolism were less in pregnant than in nonpregnant women for activities such as weeding, hoeing, pounding grain, and washing clothes.

Among agricultural workers in developing countries, there are seasonal changes in the food supply and physical work. In The Gambia during the wet season, when more people go hungry, agricultural work is greater than during the dry season, when people usually have adequate food supplies. Changes in body weight indicate that pregnant and lactating women are in a negative energy balance during the wet-hungry season and in a positive energy balance during the dry-fed season (Prentice, 1984). Thus, their body weights are relatively constant from year to year and are considered to be in long-term energy balance. Calculations of the energy available from either diet or maternal fat stores for resting metabolism and activity in pregnant and lactating women during the wet and dry seasons show that the amount of energy available is similar during both seasons, even though the energy intake is about 200 to 250 kcal less per day in the wet season. (Note: These values may be questionable as women are less likely to admit that they had sufficient food in the wet season).

The increase in the amount of energy required for walking during gestation is proportional to the maternal weight gain. The energy expended for walking (4.4 kph) in women who were in late gestation was about 0.25 kcal/minute higher than it was in nonpregnant or early-gestation women in The Gambia; the late-gestation women weighed about 5 kg more than the nonpregnant or early-gestation pregnant women (Lawrence et al., 1985). In comparison, the energy required for walking (4. 8 kph) among North American women who gained about 10 kg during pregnancy was twice as high (0.5 kcal/minute) (Nagy and King, 1983). These data suggest that the energy need for walking increases about 0.05 kcal/minute/kg of weight gain during gestation. Women who spend a significant amount of time each day walking have an additional need for energy that currently is not included in recommended energy intake for pregnant women (NRC, 1980).

Sources of Energy

The source of energy in the diet, that is, carbohydrates, protein, or fat, may be more important for physically active than for sedentary pregnant women. Glucose is the preferred fuel for the fetus, and glucose is transported across the placenta by facilitated diffusion. An adequate glucose supply for the fetus is favored by maternal increase in lipolysis during the third trimester. Glucose is also the fuel of choice for short-duration, high-intensity exercise; however, because glycogen stores are limited, fat is always an important fuel for endurance activities. Since tissue use of glucose is increased during exercise, maternal glucose levels in blood fall and may thereby limit the fetal glucose supply. In late pregnancy, glucose concentrations in blood fall with short-term exercise of moderate intensity (Gorski, 1985), suggesting that in spite of increased fat use, glucose production does not keep pace with accelerated glucose use during exercise. Changes in lactate metabolism may play a key role in these events. There may be an interspecies difference in the blood glucose response to exercise; the glucose concentration in blood was found to increase in pregnant ewes after prolonged exercise (Gorski, 1985). Studies of uterine glucose uptake are needed to determine whether a fall in the maternal glucose concentration in blood during exercise is associated with a reduction in the fetal glucose supply. Those studies may not be feasible in human, however.

To ensure the replacement of maternal glycogen stores, it may be prudent for physically active pregnant women to consume a diet high in complex carbohydrates following a period of exercise. This would allow an adequate supply of glycogen for the maintenance of maternal glucose levels in blood and the fetal glucose supply during short-term or overnight fasts.

Protein

Pregnant women retain about 6–8 g of protein (1–1.3 g of nitrogen) per day during the last half of their pregnancy. A reduction in urea synthesis and urinary urea nitrogen excretion occurs during pregnancy so that the proportion of dietary protein retained as tissue protein is higher. Since it would require that insufficient levels of protein be consumed, the efficiency of protein use in pregnant women has not been quantified. The National Research Council (1989) recommends that pregnant women consume an additional 10 g of protein per day throughout pregnancy.

Iron

Iron deficiency anemia is one of the most common nutritional problems among pregnant women. Although menstrual iron losses cease during gestation, pregnant women still require more iron than nonpregnant women do. This increased iron need, coupled with an intake of poorly absorbed iron (i.e., vegetable sources) and low maternal iron stores, accounts for the high prevalence of iron deficiency during pregnancy.

If dietary stored iron is not limiting, 800 mg of iron are deposited in maternal and fetal tissue (Bothwell et al., 1979). Of the 800 mg of iron gained, 45 percent is deposited in the conceptus and 55 percent is deposited in the expanded maternal red blood cell (RBC) mass. Blood loss at delivery and daily basal iron losses result in additional iron losses that must be provided for during pregnancy, bringing the total iron need to 1,200 mg. Since most of the expanded RBC iron is returned to the maternal stores following delivery, the net iron need during pregnancy is about 1,040 mg. The most variable of these needs is the amount required for expansion of the RBC mass, which varies with maternal iron status. In women with an unlimited iron supply, the RBC mass increases by about 35 percent; if iron is limited, the RBC mass can only expand about 18 percent (Bothwell et al., 1979).

Serum ferritin levels tend to rise postpartum, presumably due to a shift in RBC iron to the storage pool (Taylor et al., 1982). Increases in serum ferritin are greater in supplemented than in unsupplemented women, suggesting that the RBC mass expands more in the supplemented woman during gestation. Increased maternal serum ferritin levels are associated with higher serum ferritin levels in the newborn and in the 6-month-old infant, suggesting that maternal iron status does influence the amount of iron stored in the fetus (Puolakka, 1980).

To prevent depletion of maternal iron stores and to provide the needs for pregnancy, the Institute of Medicine (1990) recommends that all women take 30 mg of supplemental iron daily throughout pregnancy. Serum ferritin levels provide a rough measure of maternal iron stores during gestation. The adequacy of iron for hemoglobin formation can be estimated from erythrocyte volume measurements. A volume of less than 80 femtoliters is suggestive of iron deficiency anemia.

Pregnancy and Oxygen Consumption

Under conditions of maximal exercise, maximal oxygen consumption (VO₂-max) provides an indicator of maximal sustainable energy expenditure, and there are varying reports about whether maximal oxygen consumption can be increased in pregnant women above the level found in nonpregnant women. Recent work with pregnant women in the third trimester during treadmill exercise suggests that oxygen consumption at basal and mild work levels is increased over that in nonpregnant controls, while oxygen consumption may be significantly decreased at moderate and maximal levels of exercise (Artal, 1986). Limited data from animals suggest that some increase in VO₂-Max is possible with physical training, particularly if the training begins before pregnancy.

Pregnancy also appears to increase the biological work necessary to accomplish physical work, through increases in both total mass and respiratory work. Upper body physical activity at the same work load in pregnant and nonpregnant women appears to increase the VO ₂-max to similar degrees, while treadmill exercise involving the locomotion of gravid women appears to require more energy in pregnant than nonpregnant women, perhaps because of the larger mass carried by pregnant women.

The combination of increased resting oxygen consumption and decreased VO₂-max suggests that there is a decreased tolerance to exercise during the later part of pregnancy. The effect of conditioning before or early in pregnancy remains to be determined.

Pregnancy, Work, and Substrate Metabolism

The immediate effects of maternal physical activity on glucose metabolism are unclear. Reports of studies done in humans demonstrate increased, unchanged, or decreased serum glucose concentrations in response to maternal physical activity. Glucose turnover has not been measured in exercising, pregnant women, but the increasing respiratory quotient observed in exercising, pregnant women could be consistent with the increasing use of carbohydrates during exercise (Artal, 1981). In pregnant sheep, the maternal glucose level appears to increase with exercise (Bell et al., 1983, 1986; Lotgering et al., 1985). It is about double during treadmill exercise at about 2–3 times the RMR (Levry et al., 1982).

Hormonal Changes

Maternal hormonal responses to physical activity have received comparatively little attention, but in general, they appear to resemble the changes observed with acute stress. Mild exercise in pregnant women causes minimal hormonal changes, with a small increase in norepinephrine (Artal, 1981). More intense exercise appears to be associated with elevated epinephrine and norepinephrine, but with nonsignificant changes in plasma cortisol levels. Glucagon levels also are elevated with moderate exercise, presumably increasing hepatic glucose concentrations. Prolactin levels also increase with moderate exercise (Rauramo, 1982).

Temperature

As might be expected, maternal temperature appears to increase during physical activity. Studies in chronically catheterized sheep demonstrated small elevations in core temperature with sustained physical activity (Bell, 1986; Lotgering et al., 1985). Studies in humans suggest that the rise in core body temperature with physical activity is similar in pregnant and nonpregnant women. In pregnant as in nonpregnant animals and probably humans, exercise-induced increases in body temperature are exacerbated if ambient temperature is high. This may be an important consideration where women have to work in hot climates, especially if humidity is high, for example, wet season in The Gambia.

The placenta is an efficient exchanger of heat, as well as of gases and nutrients, and limited information suggests that physical activity-induced maternal hyperthermia appears to lead to fetal hyperthermia. Hyperthermia may, under other conditions, have effects on gas transport, metabolic rate, for teratogenicity; there also may be other effects. For example, chronic maternal hyperthermia during mid-and late gestation has profound negative effects on placental growth and transport function in sheep (Bell et al., 1987). The specific effects on the fetus of hyperthermia induced by physical activity remain unknown, however.

Effect of Maternal Undernutrition or Physical Activity on the Fetus

An acute 50-percent restriction in food intake during pregnancy in rats has a proportionately greater effect on fetal weight than on maternal weight (Lederman and Rosso, 1980). In comparison with those of pair-fed nonpregnant controls, maternal fat stores were unchanged at term, suggesting that the mothers failed to mobilize their available reserves to sustain fetal growth. Fellows and Rasmussen (1985) compared the partitioning of nutrients among acutely and chronically underfed pregnant rats. Acutely restricted dams devoted a greater proportion of the weight gain to their fetuses and had heavier litters than did chronically restricted dams. Chronically restricted dams gained both fat and protein during pregnancy, while acutely restricted dams lost fat while they maintained their protein stores at prerestricted levels. Although there is some difference in the responses of acutely versus chronically restricted dams, results of these two studies indicate that when food is restricted during gestation, a dam spares her own tissue at the cost of the fetus.

Only limited information is available regarding the effects of maternal physical activity on the fetus. For practical reasons, human data relating physical activity to fetal metabolic status are very restricted and are essentially limited to observations of the fetal heart rate.

As it has long been known, exercise induces a redistribution of blood flow that favors working muscles at the expense of splanchnic organs. A reduction of uterine blood flow of over 50 percent could potentially induce fetal asphyxia and hypoxia. Although it is believed that this happens very rarely in healthy women during mild and moderate exercise, it is possible that it may occur during strenuous and prolonged exercise (Artal et al., 1986). On the other hand, healthy fetuses may tolerate short periods of asphyxia, to which they will respond initially with an increased heart rate of 10–30 beats per minute over the normal basal rate of 140–155 beats per minute, depending on gestational age. Artal et al. (1986) have reported that in 37 pregnant women, the fetal heart rate remained significantly elevated immediately after and at 5 minutes after the end of exercise, regardless of the level of exercise; the fetal heart rate returned to the baseline 15 minutes after mild and moderate exercise, but remained elevated for at least 30 minutes after a strenuous period of exercise was stopped. Most measures of fetal responses have been taken after exercise because recording the fetal heart during exercise is technically very difficult. However, among 82 records of fetal heart rate responses during the mother's exercise, an incidence of fetal bradycardia of 8.5 percent has been reported (Artal et al., 1986). Limited information also is available on fetal breathing movements, which may increase or decrease in response to maternal physical activity, possibly in relation to maternal glucose and catecholamine responses (Platt et al., 1983).

More detailed metabolic information is available for chronically prepared sheep (Bell, 1983, 1986; Chandler, 1981, 1985; Clapp, 1980). Several observers have noted decreased uterine and, to a lesser extent, umbilical blood flow during physical activity, but oxygen uptake appears to be preserved. More recent studies have quantified the effects of physical activity on metabolism of the fetus and uteroplacenta. These studies in sheep have confirmed the observation of decreased uterine and umbilical blood flows and have documented the unchanged uterine and umbilical uptakes of oxygen, as well as the unchanged placental consumption of oxygen. Uterine glucose uptake increased, although no increase in umbilical glucose uptake was observed. Placental production of lactate showed considerable variation, while net umbilical lactate uptake appeared to decrease. These studies seem to indicate that changes in uterine blood flow need not imply that there are similar changes in nutrient flux to the placenta and fetus.

Unfortunately, no studies of the effects of maternal physical activity on fetal outcome in animals could be located.

Effects of Undernutrition on Physical Activity

Physical activity influences nutritional status and the requirements for nutrients. Individuals who regularly perform strenuous work have a higher requirement for energy than do similar individuals doing sedentary work. Conversely, the nutritional status of an individual influences his or her capacity to do work. Individuals with a reduced weight-for-height often have a compromised muscle mass and a reduced capacity to perform certain types of physical work. Also, small stature, whether due to poor nutrition during the growing years or other causes, may reduce the capacity to perform certain types of physical work later in life. In developing countries, those populations with the lowest energy intake and the highest prevalence of undernutrition are also the ones engaged in the hardest work. The effect of chronic undernutrition among these individuals on productivity, discretionary physical activity, and physical work capacity (PWC) is discussed below.

Productivity

Productivity is a utilitarian concept that involves a product with a given value as a result of work. This is different from work performance, physical activity, or work capacity, which refer to parameters independent of the measurement of the product. Time-motion studies measure energy expenditure and the contribution of physical activity to it; they may or may not be coupled to measurements of productivity in which the type of task completed and the amount of time to complete a task are reported. These studies are generally done in individuals who perform agricultural or construction work. Although impaired productivity has been documented in chronically undernourished adult male and female populations (Edmundson, 1977; Viteri, 1971; Viteri and Torun, 1974; Wolgemuth, 1982), convincing evidence on the effect of mild to moderate chronic undernutrition on a reduction of productivity or, on the other hand, of energy supplementation on an increase in productivity is not available (Immink et al., 1984; Viteri et al., 1981). This may be due to the complex biologic-economic-social interactions that define productivity (Viteri et al., 1981). For example, maintenance of productivity may be due, in part, to the subjects' desire to please the investigators (Hawthorne effect) by expending energy in excess of their intakes (Viteri and Torun, 1974). Also, payment for work may be an incentive for individuals to work beyond their comfortable level of energy expenditure to provide for family needs. Another suggested explanation for the ability of undernourished individuals to maintain productivity is that they expend less energy while performing standard work tasks than well-fed individuals do because of a higher efficiency of work. Several studies (Ashworth, 1968; Keys et al., 1950; Poole and Henson, 1988), however, have failed to find convincing evidence of improved work efficiency in underfed individuals. A reduction in basal or maintenance energy expenditure also could reduce the overall energy expenditure needed to perform work in underfed individuals. Under conditions of severe energy restriction, there is a decrease in the resting metabolic rate per unit mass of lean tissue (Keys, 1950); this decrease is more marked in the early stages of energy restriction (deBoer, 1986). However, after correction for body weight and body composition differences, the basal metabolic rates of Indian men with different socioeconomic and nutritional states did not differ (McNeill et al., 1987). Thus, there is little evidence at present that underfed individuals expend significantly less energy while performing work than well-fed individuals do.

Discretionary Physical Activity

Although nutritional status seems to have little effect on productivity, there is some evidence that it does influence discretionary physical activity. In classical studies of semistarvation, Keys et al. (1950) noted that after a 24-week period of reduced food intake, the voluntary movement of the men studied was noticeably slower. Viteri and Torun (1974) also noted a relationship between food intake and discretionary activity in Guatemalan workers. Those workers who received a 250-kcal supplement daily used their siesta to work at home, walk around town, or play football, while the unsupplemented workers rested or slept. Both groups of workers took the same amount of time to get to work each morning, but the unsupplemented workers rested more frequently on their way home from work. In a group of healthy young men from a graduate theological seminary in California, a 500-kcal/day reduction in food intake was associated with a change in physical activity (Gorsky and Calloway, 1983). Obligatory activities were not affected, but the men spent significantly less time standing at leisure and walking and more time sitting at leisure. These data suggest that an early response to limited food intake is a reduction in discretionary activity, if time for discretionary activity exists. However, the data in Chapter 2 of this report indicate that rural Guatemalan women who perform agricultural work but who are also responsible for household work and child care spend only 25 percent, (6 hours) of their day off their feet. These women seem to have no discretionary time at all after allowing for sleep. The activity patterns of women given energy supplements during pregnancy and lactation have not been compared with those of unsupplemented women, but it has been observed that those women who receive energy supplements seem to have more energy for singing and talking while working in the fields (Prentice et al., 1983).

Physical Work Capacity (PWC)

PWC is quantitated by determining the maximal capacity to consume oxygen (VO₂-max) or the endurance time while performing standardized work: that is, the time it takes an individual to walk on a treadmill or ride a bicycle ergometer at a defined speed and grade. A restriction in food intake, either acute or chronic, seems to cause a significant depression in the VO₂-max. A 580 or 1,010-kcal/day restriction for 24 days caused a 5–10 percent reduction in VO₂-max; this decrease was proportional to the decrease in body weight (Taylor, 1957). The VO₂-max of chronically malnourished adults in Guatemala and Colombia was depressed to the same degree as the depression of muscle cell mass (Spurr, 1984); more than 80 percent of the difference in VO₂-max between subjects with mild or severe malnutrition was accounted for by differences in muscle mass. While endurance time did not seem to be related to nutritional status among the subjects studied (Spurr, 1984), an unexplained reduction in the time required to become fatigued was seen in severely malnourished individuals after they had completed 2.5 months of dietary repletion. It is unclear why repletion with a nutritionally adequate diet caused a reduction in endurance time. There are very few studies of the effect of malnutrition on endurance time. More work is needed in this area.

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