5
Effects of Diet and Physical Activity in Pregnant Human Populations

This chapter reviews the epidemiologic evidence concerning the effects of maternal energy intake and physical activity on pregnancy. Three different aspects of maternal energy balance are considered: nutrition during gestation, maternal physical activity, and the combined effects of nutrition and physical activity during gestation. Where available data permit, these three aspects will be examined with respect to the following fetal, infant, and maternal outcomes: fetal growth, gestational duration, spontaneous abortion (miscarriage), congenital anomalies, maternal mortality, and other pregnancy complications.

Far more studies have focused on fetal growth and gestational duration than on the other outcomes; consequently, these will receive more attention here. Fetal growth and gestational duration are the two determinants of birth weight, and from an international health perspective, birth weight is the most readily available index of pregnancy outcome. It is also a useful general indicator of women's health before and during pregnancy and of adverse influences on the developing fetus (See Table 2-3).

Much of the material in this chapter that bears on the determinants of fetal growth and gestational duration is taken from a recent review (Kramer, 1987) based on a methodologic assessment and synthesis of 895 articles in English and French published between 1970 and 1984. These papers described 43 factors that may act as determinants of intrauterine growth retardation or short gestation. A list of the studies examined in this review has been published (Kramer and Sasportas, 1985). The methodologic criteria used in evaluating studies bearing on maternal energy intake, physical activity, and gestational weight gain are shown in Tables 5-1a and 5-1b. For physical activity, the review has been updated (using the same criteria) to



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Nutrition Issues in Developing Countries: Part I: Diarrheal Diseases - Part II: Diet and Activity During Pregnancy and Lactation 5 Effects of Diet and Physical Activity in Pregnant Human Populations This chapter reviews the epidemiologic evidence concerning the effects of maternal energy intake and physical activity on pregnancy. Three different aspects of maternal energy balance are considered: nutrition during gestation, maternal physical activity, and the combined effects of nutrition and physical activity during gestation. Where available data permit, these three aspects will be examined with respect to the following fetal, infant, and maternal outcomes: fetal growth, gestational duration, spontaneous abortion (miscarriage), congenital anomalies, maternal mortality, and other pregnancy complications. Far more studies have focused on fetal growth and gestational duration than on the other outcomes; consequently, these will receive more attention here. Fetal growth and gestational duration are the two determinants of birth weight, and from an international health perspective, birth weight is the most readily available index of pregnancy outcome. It is also a useful general indicator of women's health before and during pregnancy and of adverse influences on the developing fetus (See Table 2-3). Much of the material in this chapter that bears on the determinants of fetal growth and gestational duration is taken from a recent review (Kramer, 1987) based on a methodologic assessment and synthesis of 895 articles in English and French published between 1970 and 1984. These papers described 43 factors that may act as determinants of intrauterine growth retardation or short gestation. A list of the studies examined in this review has been published (Kramer and Sasportas, 1985). The methodologic criteria used in evaluating studies bearing on maternal energy intake, physical activity, and gestational weight gain are shown in Tables 5-1a and 5-1b. For physical activity, the review has been updated (using the same criteria) to

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Nutrition Issues in Developing Countries: Part I: Diarrheal Diseases - Part II: Diet and Activity During Pregnancy and Lactation include studies published since 1984. In addition, other maternal and infant outcomes also have been considered. TABLE 5-1a Methodologic: Standards Used To Assess Published Studies Bearing on Maternal Energy Intake, Physical Activity, and Gestational Weight Gain   Gestational Weight Gain Physical Activity Energy Intake Definition of Target Population and Study Sample X X X Description of Study Participation and Follow-Up Rates X X X Demonstration of Appropriate Temporal Sequence Between Factor and Outcome X   X Use of Experimental Design     X TABLE 5-1b Confounding Variables Requiring Control Used To Assess Published Studies Bearing on Maternal Energy Intake, Physical Activity, and Gestational Weight Gain Racial/Ethnic Origin X   X Maternal Height   X X Prepregnancy Weight X X X Maternal Agea X X X Socioeconomic Status X X X Energy Intake   X   Physical Activity     X Protein Intake     X Cigarette Smoking X X X Alcohol Consumption X X X a Parity was accepted as a proxy control variable for maternal age. EFFECT OF ENERGY INTAKE Background An important issue in studying energy intake is the difficulty in measuring it. Energy intake measurement requires either prolonged and careful observation, which may in itself influence energy intake, or adequate subject recall of dietary intake. Even if individual measurements are valid and reproducible, measurements must be made repeatedly during pregnancy to ensure that the entire gestational period is covered.

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Nutrition Issues in Developing Countries: Part I: Diarrheal Diseases - Part II: Diet and Activity During Pregnancy and Lactation The susceptibility of energy intake to experimental intervention also deserves consideration. Random assignment of energy supplementation is feasible and provides the best methodologic approach for assessing the effects of energy intake, provided that caloric substitution and net caloric increase are also taken into account. Consequently, the best epidemiologic data available concerning the effects of energy intake are those based on supplementation trials or careful observational studies of several ''natural'' experiments involving severe caloric restriction (i.e., famines) in previously well-nourished women. In the absence of a randomized experimental design, it is important to consider factors that may confound the relationship between energy intake and pregnancy outcome, that is, factors associated with energy intake and pregnancy outcome independent of energy intake. The potential confounding variables that should be controlled include racial or ethnic origin, socioeconomic status, age, parity, height, prepregnant nutritional and health status, and cigarette and alcohol consumption. In developing countries, a control for infectious morbidity during pregnancy is also important because it can be associated with both reduced energy intake and impaired fetal growth. Even chronic infestation with intestinal nematodes and protozoans may affect the efficiency of nutrient use and could act as an important confounding variable. Because women who consume more energy often burn more energy, a valid assessment of the effect of energy intake on pregnancy outcome requires careful monitoring of energy expenditure. The length of gestation is itself an essential control variable because women who deliver their infants preterm will have consumed less total energy (an example of temporal precedence [reverse causality] bias). The effect of energy intake on gestational duration should, therefore, be based on the daily intake rather than overall intake. Effects on fetal growth either should be based on a similar measure (e.g., daily energy intake) or should control for gestational age. In addition to its role as a potential confounding variable, prepregnant nutritional status, as reflected in prepregnancy weight, weight-for-height, or skinfold thickness, is also likely to modify the effect of energy intake on fetal growth. In other words, it might be expected that thin women would derive a greater increase in birth weight for a given intake of energy than would well-nourished or overnourished women. This hypothesis would predict that in women who begin pregnancy with large fat stores, energy intake would have little if any effect on fetal growth.

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Nutrition Issues in Developing Countries: Part I: Diarrheal Diseases - Part II: Diet and Activity During Pregnancy and Lactation Gestational Duration Few epidemiologic studies have examined the effects of energy intake on gestational duration. In fact, only two reports (Delgado et al., 1982; Villar et al., 1986) found a significant association, and those, though more recent and based on a larger sample, contradicted two previous reports of the same study of energy supplementation in Guatemala (Habicht et al., 1974; Lechtig et al., 1975). No effect on mean gestational age or rate of preterm delivery was reported in other energy supplementation trials (McDonald et al., 1981; Rush et al., 1980). Although historical evaluation of the effects of food supplements given to eligible women as part of the Special Supplemental Food Program for Women, Infants, and Children (WIC) program reported a significant increase in mean gestational age and a significant reduction in both preterm and very preterm (< 33 weeks) births, a concurrent (longitudinal) study found smaller, nonsignificant effects (Rush et al., 1988a and 1988b). Thus, although most of the available data suggest that maternal caloric intake does not have a large effect on gestational duration, a small effect cannot be excluded. It is also important to understand that most studies bearing on gestational duration have based their assessment of gestational age on the mother's recollection of her last menstrual period. Compared with the "gold standard" of early ultrasonographic measurement of the biparietal diameter, low last menstrual period gestational age estimates tend systematically to underestimate true gestational age, whereas the reverse is true for high (i.e., postterm) last menstrual period estimates (Kramer et al., 1988). The end result will be some inevitable misclassification of growth-retarded infants as preterm (and vice versa). Fetal Growth Research on fetal growth reveals a different picture from that provided above. Examination of the evidence from the better designed and controlled epidemiologic studies (primarily the supplementation trials) reveals that there is an increase in the gestational age-adjusted birth weight of pregnant women given energy supplements (Blackwell et al., 1973; Herrera et al., 1980; McDonald et al., 1981; Mora et al., 1973; Prentice et al., 1983; Rush et al., 1980; Viegas et al., 1982). The only exception to this general pattern is the previously cited update of the Guatemala study (Villar et al., 1988), which found no reduction in risk of intrauterine growth retardation in energy supplemented women. The effect on fetal growth appears to be conditional on the women's nutritional status before pregnancy. In

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Nutrition Issues in Developing Countries: Part I: Diarrheal Diseases - Part II: Diet and Activity During Pregnancy and Lactation supplementation trials with demonstrably undernourished subjects, the effect of a given daily energy intake was greater than the effect in better nourished women. The data are somewhat mixed on the importance of the timing of the energy intake during pregnancy. Although most of the evidence regarding supplementation suggests that it is effective at any time during gestation (Habicht et al., 1974; Prentice et al., 1983), the Dutch famine study (Stein et al., 1975) showed that energy deprivation is important only in the third trimester. Hytten and Chambers (1980) have also found that energy requirements are considerably higher during the second and third trimesters than in the first trimester. Many of the participants in the supplementation studies did not begin supplementation until the second trimester, and it is unclear whether the reported effects of later supplementation would have had the same effects earlier in gestation. Quantitative estimates of the effect of energy supplementation on fetal duration and fetal growth are summarized in Table 5-2. TABLE 5-2 Effect of Energy Supplementation on Gestational Age, Preterm Birth, Birth Weight, and Intrauterine Growth Retardation Outcome   Effect Gestational Age   None Preterm Birth   None Birth Weight In women poorly nourished before pregnancy 99.7 g/100 kcal/day supplemented throughout pregnancya   In women well-nourished before pregnancy 34.6 g/100 kcal/day supplemented throughout pregnancya Intrauterine Growth In women poorly nourished before pregnancy RRb: 0.47 Retardation In women well-nourished before pregnancy RRb: 0.82 a Throughout pregnancy indicates that the supplement is given for 280 days. Durations of supplementation shorter than 280 days would require proportionately more calories per day. b RR: Relative risk of intrauterine growth retardation in women who receive 100 supplemented calories per day throughout pregnancy versus women who receive no caloric supplement. SOURCE: Kramer, 1987. Spontaneous Abortion Epidemiologic studies of spontaneous abortion (miscarriage) are notoriously difficult, in particular because early miscarriages may not be recognized, and even if they are recognized, they may not come to the attention of a physician or other health care worker. The subcommittee identified few data relating spontaneous abortion and maternal nutrition.

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Nutrition Issues in Developing Countries: Part I: Diarrheal Diseases - Part II: Diet and Activity During Pregnancy and Lactation In an early study of the effects of the Dutch famine, Smith (1947) noted an increased rate of "abortion and miscarriage" for Rotterdam women who conceived during the famine, but it is not clear whether the reported figures include induced abortions. Smith comments on the data presented by saying "there is no reason to assume they are accurate or that conclusions can be drawn from them." A hospital-based study from New York City tried to identify relationships between prepregnant nutritional status and all forms of spontaneous abortions, including those of a particular chromosomal type. It found no associations (Stein, 1989). The hospital-based study from New York City found no association of spontaneous abortion with prepregnant nutritional status (Kline and Stein, 1987). A prospective study of pregnancies in Bangladesh reported that conception during the "lean period" (a period from June to October encompassing a phase of arduous work and reduced diet) was associated with pregnancy loss primarily in the third trimester, but before and during the second trimester as well (Pebley et al., 1985). Congenital Anomalies The subcommittee found no data relating gestational energy intake to the risk of congenital anomalies, in general, or of specific malformations. Deficiencies in specific nutrients have been linked to endemic goiter caused by iodine deficiency, and neural tube defects have been linked to lack of folate or B vitamins. Such specific deficiencies were considered to be outside the mandate of the subcommittee. Maternal Mortality In most developed countries, maternal mortality during pregnancy or childbirth is extremely rare, with rates generally below 10 per 100,000. The most common causes are pregnancy-related hypertension, pulmonary embolism, ectopic pregnancy, and hemorrhage (ante-and postpartum) (NCHS, 1987). In the United States, rates are 3–4 times higher for black women than for white women (Buehler et al., 1986). This discrepancy appears to be associated with poor prenatal care among black women (Sachs et al., 1987). Nutritional differences might also explain part of the racial discrepancy; but many other explanations are possible, and neither energy intake nor other nutritional factors have been investigated directly. In sharp contrast, maternal mortality rates in developing countries are 10–50 times higher (in extreme cases, they may be up to 550 times higher)

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Nutrition Issues in Developing Countries: Part I: Diarrheal Diseases - Part II: Diet and Activity During Pregnancy and Lactation (WHO, 1987), and the principal causes are hemorrhage, infection, and toxemia. Although none of these causes has been associated directly with maternal nutrition, one might speculate that women who were anemic on a nutritional basis would be more likely to the from hemorrhage before, during or after childbirth. Finally, heart failure during and after childbirth can occasionally lead to maternal death. This has been observed principally but not exclusively among the poor in the United States, Africa, and elsewhere (Demakis and Rahimtoola, 1971). Although this observation could have a nutritional explanation, no direct evidence for this has been adduced (Homans, 1985). Other Pregnancy Complications No studies have produced convincing evidence directly linking maternal energy intake to either toxemia or dystocia (Davies and Dunlop, 1983; WHO, 1965). However, an observed reduction in eclampsia in Germany was temporally associated with food shortages during World War I (Anonymous, 1917; NRC, 1970). As discussed above, energy intake is associated with fetal growth. Thus low intake would be expected to reduce the risk of high birth weight (> 4,000 g) and the corresponding increased risk of dysfunctional labor, forceps delivery, birth trauma, and Caesarean section (Koff and Potter, 1979; Modanlou et al., 1980; Boyd et al., 1983), particularly in women with short stature or small pelvic size (Frame et al., 1985; Hughes et al., 1987). In general, undernutrition is associated with lower blood pressure, and as has been discussed above, gestational undernutrition impairs fetal growth. For example, the severe energy restriction that occurred during the Dutch famine was associated with a significant reduction in systolic blood pressure near the time of delivery (Riberiro et al., 1982). Although this might represent some reduction in the risk of toxemia, it could also be a mechanism for lowering uterine blood flow and thereby impairing fetal growth. EFFECTS OF MATERNAL WORK AND PHYSICAL ACTIVITY Background As reviewed in Chapter 2, maternal energy expenditure in rural developing settings is of major interest because women in such countries often engage in strenuous activities, even during pregnancy, and because it is closely linked to adequate energy intake. Maternal work itself might also

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Nutrition Issues in Developing Countries: Part I: Diarrheal Diseases - Part II: Diet and Activity During Pregnancy and Lactation have an effect on pregnancy outcome quite separate from its effect on energy balance. For example, maternal physical activity or posture during work might diminish uterine blood flow and, consequently, hinder the fetal oxygen and nutrient supply (see Chapter 4). Moreover, there is some evidence that even quiet standing can provoke uterine contractions late in gestation (Schneider et al., 1985), which could theoretically increase the risk of preterm labor. Physical fatigue and psychological stress may be greater for women engaging in some types of work and may thereby affect pregnancy outcome. Exercise-induced hyperthermia could affect cellular differentiation and organogenesis during critical periods of development. Finally, exposure to toxic substances in the work environment may also affect pregnancy performance and outcome. In examining the epidemiologic evidence, researchers should adapt the methodologies to the particular aspect of maternal physical activity under consideration. If the focus is on energy expenditure or strenuous physical labor, energy intake is an important potential confounding variable because the net balance of available energy depends on both energy intake and expenditure. When food supply is not a limiting factor, women who burn more energy also are likely to eat more, but failure to control energy intake may yield spurious results. Other factors that may confound the effect of energy expenditure include age, parity, height, prepregnancy weight, general health status, racial or ethnic origin, socioeconomic status, and smoking and alcohol consumption. In considering the effects of posture, fatigue, stress, physical fitness, hyperthermia, or other aspects of maternal physical activity on pregnancy, energy intake need not be controlled; however, other potential confounding factors would be similar to those mentioned above. In assessing data from developed countries, it should be borne in mind that women who engage in leisure-time sports activities and exercise are likely to be younger, better nourished, and of higher socioeconomic status and are less likely to be members of a racial minority than those who do not. They are also much less likely to smoke or drink. And because intensive sport or exercise entails considerable energy expenditure, energy intake should also be controlled when assessing its effects. In examining the available evidence from such studies in developed countries, it is often difficult to separate the effects of energy expenditure from non-energy-related work factors. Many of the reports from developed countries, for example, entailed studies of maternal work as a dichotomous variable, comparing pregnancy outcomes in women with paid employment with those in women without paid employment during pregnancy. Many of these reports have not distinguished different types of work in terms of physical exertion, posture, fatigue, or stress. By contrast, studies from

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Nutrition Issues in Developing Countries: Part I: Diarrheal Diseases - Part II: Diet and Activity During Pregnancy and Lactation developing countries make it apparent that maternal work often involves considerable energy expenditure in addition to any effects that are not energy related. Gestational Duration The evidence concerning physical activity and gestational age is conflicting. Two fairly well-controlled studies from a single data base in The Gambia found no significant effects of heavy agricultural labor on mean gestational age (Prentice, 1980; Prentice et al., 1981). A recently published study from Zaire (Manshande et al., 1987), on the other hand, reported significantly longer gestations in full-term (> 38 weeks) female infants born to hard-working multiparous women with longer durations of stay in a maternal rest village. No such effect was seen in male infants, however, and even the reported effect in females may reflect a temporal precedence (reverse causality) bias in that women who delivered earlier had less time to spend in the rest village. The evidence from developed countries is more abundant but equally conflicting. A study of women in Boston found no effect of maternal employment in jobs requiring standing, even when the job was continued into the third trimester (Zuckerman et al., 1986). Although a variety of potentially confounding variables were controlled in the study, it is possible that women who continue to work are likely to be those without pregnancy difficulties, a factor that could explain the findings. By contrast, Clapp and Dickstein (1984) found that Vermont women who continued endurance-type exercise, including jogging, cross-country skiing, or aerobic dancing, during the third trimester of pregnancy had significantly shorter gestations than those who were either sedentary or stopped vigorous exercise of this kind before the third trimester. These results should be interpreted with caution, however, since they are based on only 29 women who continued exercising, and several potentially confounding variables were incompletely controlled. Jarrett and Spellacy (1983) reported on 67 trained women runners who responded to a notice published in a Chicago newspaper and completed a mailed postpartum questionnaire concerning jogging during pregnancy and pregnancy outcome. There was no significant correlation between the total number of miles run during pregnancy or during the third trimester and gestational age at delivery. However, the method of subject recruitment (perhaps selecting high-mileage runners with more favorable outcomes); the fact that women who allowed themselves to run more miles may have been those whose pregnancies were uncomplicated and proceeding well; and the failure to control the potentially confounding effects of maternal age, height,

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Nutrition Issues in Developing Countries: Part I: Diarrheal Diseases - Part II: Diet and Activity During Pregnancy and Lactation prepregnancy weight, energy intake, smoking, parity, racial/ethnic origin, and socioeconomic status limit any causal inferences that can be drawn from this study. Most of the data regarding preterm labor and delivery come from developed countries. Berkowitz et al. (1983) found no elevation in risk of delivery in working mothers after potential confounding variables were controlled, and there were no bivariate associations among preterm delivery and any of the following: physical position during work, lifting or carrying, weights of loads, frequency of lifting, number of hours worked, hours of housework per week, the use of an assistant for housework, climbing stairs, or hours of child care per work week. In fact, light and moderate leisure-time physical activity was associated with a significantly reduced risk of preterm birth. More strenuous exercise appeared to increase the risk, however. Although not statistically significant, this latter finding is consistent with that reported by Clapp and Dickstein (1984). A problem with the study of Berkowitz et al. (1983) concerns the measure of gestational age, which was based on the Dubowitz score, a measure of neurologic development, rather than the date of the mother's last menstrual period. In one well-controlled study, Mamelle et al. (1984) reported an elevated risk of preterm delivery among working women whose work involved tiring postures, work on industrial machines, physical exertion, mental stress, or a physically uncomfortable environment. Because these work-related aspects were combined, however, it is difficult to separate the effects of fatigue and psychological stress. In a more recent attempt to validate their original findings, Mamelle and Munoz (1987) found a significantly increased risk of preterm delivery in women with an elevated summary occupational "fatigue score," but it is unclear what (if any) confounding factors were controlled in their analysis. A recent, well-controlled interview survey of Montreal women employed for 30 or more hours a week at conception attempted to relate the risk of preterm birth to type of occupation and adverse working conditions. Modest increases in risk (relative risks of 1.25–1.35) were associated with long hours (> 46 hours/week) and lifting heavy weights, both in women who stopped working before 28 weeks and those who continued working beyond 28 weeks. Psychiatric nurses had a particularly high risk of preterm delivery (relative risk of 2.47), but the large number of occupations examined suggests the need for caution in interpreting this intriguing result (McDonald et al., 1988). A recent Finnish study (Nurminen and Kurppa, 1988) found no difference in mean gestational age or rate of preterm birth in office versus nonoffice workers. Neither group was compared to women who did not work during pregnancy, however, nor did the investigators stratify

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Nutrition Issues in Developing Countries: Part I: Diarrheal Diseases - Part II: Diet and Activity During Pregnancy and Lactation the type of office work by exertion, stress, or other factors (other than users versus nonusers of video display terminals). In two reports based on the U.S. National Longitudinal Survey of Labor Market Experience, Homer et al. (in press) examined the relationship between preterm, low-birthweight (LBW) delivery and work experience among 2,400 young women. Women who worked during pregnancy were at significantly lower risk for delivering a pretem, LBW infant than those who did not work, even after controlling confounding differences in race, socioeconomic and marital status, maternal height, prior history of LBW infants, and commencement of first prenatal care. Among women who worked, however, those with jobs associated with high physical exertion or psychological stress (jobs with high-demand tasks but low individual control) were at increased risk for preterm, LBW delivery when each factor was considered alone. When these two job characteristics were considered together along with potential confounders in a multivariate model, only physical exertion remained significant, with a six-fold increased risk of preterm, LBW delivery. The studies discussed above are the best in the literature from a methodologic standpoint Unfortunately, other studies, which have been less well controlled, do not help settle the issue of whether maternal work or physical activity increases the risk of preterm delivery. Kaminski et al. (1973) found no increased risk of preterm delivery in women who said they had worked outdoors during pregnancy. Similarly, Murphy et al. (1984) reported no significant difference in preterm delivery rates in women with and without paid employment during pregnancy. A reanalysis of the same data by Williams (1984) showed a significantly reduced risk of pretem delivery in the employed women. Two reports of a single French study found a reduced risk of preterm delivery in working women, although women working more than 42 hours a week and those who worked in a standing position had an increased risk (Saurel and Kaminski, 1983; Saurel-Cubizolles et al., 1982). In a recent study of nonphysician hospital workers carried out by the same group of French investigators, the duration of the work week and commuting time had no effect on the preterm birth rate (Saurel-Cubizolles et al., 1985). Ancillary workers involved in strenuous cleaning, carrying heavy loads, and prolonged standing had higher preterm delivery rates; however, after controlling for differences in ethnic origin, these differences were no longer statistically significant. A more recent report by the same group of French researchers found that employed immigrant women, most of whom work in manual and service jobs requiring that they carry heavy loads or remain in a standing position or both, had no increased risk of preterm delivery (Stengel et al., 1986). These results, however, were not adjusted for the higher socioeconomic status, greater number of prenatal

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Nutrition Issues in Developing Countries: Part I: Diarrheal Diseases - Part II: Diet and Activity During Pregnancy and Lactation Picone et al. (1982) compared women with predicted low (< 15 lbs) and adequate (> 15 lbs) total weight gains, where the prediction was based on weight gain at 20 weeks gestation of < 8 versus > 8 lbs. There was no difference in mean gestational age between the two groups when based on the mother's last menstrual period (LWP), but a slightly shorter (38.5 versus 39.2 weeks; P < .01) gestational age based on neonatal (Dubowitz) examination. These results are even more difficult to interpret in light of the fact that the investigators "reclassified" two of the women whose ultimate total weight gains did not agree with their predictions at 20 weeks. Based on the large Child Health and Development Studies in the San Francisco Bay area, Bracken (1984) reported a highly significant increased risk of preterm birth (based on LMP) in women with weight gains averaging < 0.5 lbs/week after 20 weeks gestation. These results are closely paralleled by those in a recent study by Abrams et al. (in press), in which an increased risk of preterm delivery was seen in women with a low (< 0.27 kg/week) rate of weight gain (a 60-percent increase in risk over women gaining 0.27–0.52 kg/week). Of note is the fact that the magnitude of elevated risk reported in the latter study was not materially altered when the analysis was restricted to preterm births whose gestational ages were confirmed by ultrasound examination before 28 weeks. Finally, two other reports of a recent study among adolescents (Hediger et al., 1989) also found that a low rate of GWG was associated with preterm delivery. The magnitude of the increased risk varied from 50–75 percent, depending on whether the gestational age was based on the last menstrual period or an "obstetric" (undefined) estimate. The risk appeared to be even higher if the low gain occurred both before and after 24 weeks. One important methodologic caveat should be kept in mind in interpreting studies linking GWG to gestational duration. As discussed earlier in the section on the effect of energy intake, errors in estimation of gestational age (particularly when based on menstrual dates) may well lead to misclassification of some growth-retarded infants as preterm. Since GWG has been shown to have an effect on fetal growth and the risk of IUGR (vide infra), evidence of effects on gestational duration that are based on menstrual dates should be interpreted with caution. Even with this caution, however, some existing data do suggest a possible effect of low weight gain on reducing gestational duration and increasing the risk of preterm delivery. Further research in this area using validated (e.g., based on early ultrasound) gestational age measurements should receive high priority, given the well-known importance of preterm delivery on infant mortality and infant and child morbidity and performance.

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Nutrition Issues in Developing Countries: Part I: Diarrheal Diseases - Part II: Diet and Activity During Pregnancy and Lactation Fetal Growth The data are clearer concerning an effect of GWG on intrauterine growth. All of the methodologically acceptable studies the subcommittee examined reported a positive effect of GWG on gestational age-adjusted birth weight and a reverse effect on the risk for intrauterine growth retardation. The causal effect of maternal gestational weight gain on birth weight may have been overestimated, however, since few of the examined studies subtracted the weight of the newborn from the maternal weight gain in assessing the association between GWG gain and birth weight. Although most of the studies originated from privileged populations in developed countries, studies in Peru (Frisancho et al., 1984) and in a sample of black women of low socioeconomic status in New York City (Rush et al., 1972) reported similar results. Investigators examining the effect of a given GWG in women of varying prepregnant nutritional status have been virtually unanimous in concluding that the two factors strongly interact. Miller and Merritt (1979), for example, showed a clear trend for increasing rates of intrauterine growth retardation with decreasing pregnant weight-for-height among women with low GWG. Similar results were reported in several studies investigating mean birth weight (Abrams and Laros, 1986; Mitchell and Lerner, 1989; Naeye, 1981a,b; Winikoff and Debrovner, 1981). Thus, it seems clear that undernourished women receive a greater benefit from a given GWG than do those who are adequately or over-nourished. The effect of modification of prepregnancy nutritional status could be of major importance in developing countries. Because a large proportion of pregnant women can be expected to be undernourished in such a setting, low GWG may be a major risk factor for IUGR. Quantitative estimates of the effects of GWG are summarized in Table 5-3 (Kramer, 1987). These estimates derive from studies in women with adequate prepregnancy nutritional status. Although the effects are likely to be considerably greater in undernourished women, available data do not permit accurate quantitative estimates. Other Pregnancy Outcomes High weight gains, particularly in the second and third trimesters, have long been associated with an increased risk of pregnancy-induced hypertension and pre-eclampsia (toxemia) in primiparae (Tompkins et al., 1955; Thomson and Billewicz, 1957; Naeye, 1981a; Shepard et al., 1986). In fact, recognition of this association reinforced the earlier obstetric practice of

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Nutrition Issues in Developing Countries: Part I: Diarrheal Diseases - Part II: Diet and Activity During Pregnancy and Lactation limiting weight gain, which appears to have originated with the previously noted observed reduction in eclampsia in Germany that was temporally associated with food shortages during World War I (Anonymous, 1917; NRC, 1970). But sorting out the "cart" and the "horse" in this association is highly problematic because the edema and increased body water accompanying pre-eclampsia will, of course, be manifested by an increased maternal weight, irrespective of any change in maternal lean or fat mass. The typical pattern is a sudden increment in weight between visits in the third trimester. TABLE 5-3 Effect of Gestational Weight Gain (GWG) on Gestational Age, Preterm Birth, Birth Weight, and Intrauterine Growth Retardation for Women with Adequate Prepregnancy Nutrition Outcome Effect Gestational Age None Preterm Birth None Birth Weight 20.3 g/kg total GWG Intrauterine Growth Retardation RRa: 1.98 aRR: relative risk of intrauterine growth retardation in women with total gestational weight gain <7 kg versus those with gestational weight gain > 7 kg. SOURCE: Kramer, 1987. The subcommittee was unable to locate any evidence linking increases in maternal lean or muscle mass early in pregnancy to subsequent pre-eclampsia. In fact, an expert committee of the World Health Organization concluded "that it is difficult on the evidence available to define the precise role of nutrition in toxaemia" (WHO, 1965). Tompkins et al. (1955) did note a higher risk of toxemia in women with low prepregnancy weight-for-height who had low weight gains during the second trimester. In his review of the published evidence, Chesley (1976) found that, despite the cart-versus-horse bias discussed above, most women who develop pre-eclampsia have total weight gains below average. Thus, the causal relationship between GWG and pre-eclampsia remains unclear. Low early gains may be a marker, or even a determinant, of subsequent pre-eclampsia, but firmer inferences must await the results of future research. Large GWGs are associated with an increased risk of high birth weight, with a corresponding increase in risk for dysfunctional labor, midforceps delivery, birth trauma, asphyxia, and Caesarean section (Koff and Potter, 1939; Modanlou et al., 1980; Boyd et al., 1983). Moreover, there is some

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Nutrition Issues in Developing Countries: Part I: Diarrheal Diseases - Part II: Diet and Activity During Pregnancy and Lactation evidence that these consequences of fetopelvic disproportion are exacerbated in women with short stature or small pelvic size (Frame et al., 1985; Hughes et al., 1987). Varma (1984) has examined the direct relationship between gestational weight gain and pregnancy complications. Although he reports a significantly higher rate of forceps delivery and Caesarean section in women with high weight gains, these results are unadjusted for potentially confounding differences among women with different weight gains. Using a more sophisticated multivariate approach, however, Shepard et al. (1986) confirmed that women with high weight gains (measured as a proportion of prepregnancy weight) had higher rates of Caesarean sections and other operative deliveries (forceps and vacuum extraction). They also found such women to have a prolonged second stage of labor. DIRECT EVIDENCE OF COMBINED EFFECTS Previously cited studies from The Gambia have also provided some direct evidence concerning the combined effects of low energy intake and high energy expenditure (Prentice, 1980; Prentice et al., 1981). As discussed earlier, these studies found a substantial decrement in birth weight during the wet season, when food availability is lowest and agricultural labor demands are highest. Prentice et al. (1981) documented a difference in birth weight between the wet and dry seasons of 240 gm, a mean of 2,740 gm in the wet season and 2,980 gm in the dry season. These findings were somewhat surprising because the differences in energy intake were only about 200 kcal/day and persisted for only a few months. Averaged over the entire pregnancy, there were only modest differences in energy intake. Although energy intake is difficult to measure with precision, the difference in birth weight is much greater than would be predicted from the difference in energy intake alone, even among poorly nourished women (see Table 5-2). The additional birthweight effect might therefore be attributable to increased energy expenditure during the wet season. Unfortunately, however, this effect is likely to be confounded with a higher prevalence of malarial illness during the wet season, which is also likely to decrease birth weight. Similar results of a smaller magnitude were reported from Taiwan (Adair and Pollitt, 1983). Birth weights were significantly lower in the summer rainy season, when food availability is low and both agricultural activity and infectious morbidity (particularly from gastroenteritis) are high. However, as in The Gambia, it is not possible to distinguish the individual and combined effects of the various seasonally related factors.

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Nutrition Issues in Developing Countries: Part I: Diarrheal Diseases - Part II: Diet and Activity During Pregnancy and Lactation Few investigators have examined the actual interactions (i.e., effect modification) between maternal physical activity and nutritional status before or during pregnancy. Studies by Tafari et al. (1980) in Ethiopia, and by Naeye and Peters (1980) using data from the U.S. Collaborative Perinatal Project both found a greater reduction in birth weight attributable to maternal work in women with low prepregnant weight and gestational weight gain. Interestingly, Naeye and Peters (1982) attributed this effect to the higher frequency of placental infarcts found in women whose work required them to stand and continued into late gestation. No such infarcts were observed in the Ethiopian study, however, despite the expectation of more strenuous physical work in the latter setting (Tafari et al., 1980). The studies described above suggest an interaction that is potentially highly significant for the development of public policies and programs regarding maternal nutrition and strenuous work. As was described in Chapter 2, many women in developing countries are undernourished and must continue to perform work activities that include heavy energy expenditure throughout pregnancy. Further study of this interaction should receive high priority in future epidemiologic research. REFERENCES Abrams, B.F., and R.K. Laros, Jr. 1986. Prepregnancy weight, weight gain, and birth weight. Am. J. Obstet. Gynecol. 154:503–509. Abrams, B.F., V. Newman, T. Key, and J. Parker. 1989. Maternal weight gain and preterm delivery. Obstet. Gynecol. 74(4):577–583. Adair, L.S., and E. Pollitt. 1983. Seasonal variations in pre-and postpartum maternal body measurements and infant birth weights. Am. J. Phys. Anthropol. 62:325–331. Anonymous. 1917. Eclampsia rare on war diet in Germany (editorial). J. Am. Med. Assoc. 68:732. Armstrong, B.G., A.D. Nolin, and A.D. McDonald. 1989. Work in pregnancy and birth weight for gestational age. Br. J. Ind. Med. 46:196–199. Beral, V., J.A. Grisso, and E. Roman. 1985. Is paid employment during pregnancy detrimental to the offspring? Pp. 261–264 in M. Marois, ed. Prevention of Physical and Mental Congenital Defects. Proceedings of an International Conference of the Institut de la Vie. Alan R. Liss, New York. Berkowitz, G.S. 1981. An epidemiologic study of preterm delivery. Am. J. Epidemiol. 113:81–92. Berkowitz, G.S., J.L. Kelsey, T.R. Holford, and R.L. Berkowitz. 1983. Physical activity and the risk of spontaneous preterm delivery. J. Reprod. Med. 28:581–588. Blackwell, R.Q., B.F. Chow, K.S.K. Chinn, B.N. Blackwell, and S.C. Hsu. 1973. Prospective maternal nutrition study in Taiwan: Rationale, study design, feasibility, and preliminary findings. Nutr. Rep. Int. 7:517–532. Boyd, M.E., R.H. Usher, and F.H. MacLean. 1983. Fetal macrosomia: Prediction, risks, proposed management. Obstet. Gynecol. 61:715–722. Bracken, M.B., ed. 1984. Perinatal Epidemiology. Oxford University Press, New York. 550 pp. Briend, A. 1980. Maternal physical activity, birth weight, and perinatal mortality. Med. Hypotheses 6:1157–1170.

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Nutrition Issues in Developing Countries: Part I: Diarrheal Diseases - Part II: Diet and Activity During Pregnancy and Lactation Buehler, J.W., A.M. Kaunitz, C. Hogue, J.M. Hughes, J.C. Smith, and R.W. Rochat. 1986. Maternal mortality in women aged 35 years or older: United States. J. Am. Med. Assoc. 255:53–57. Cherry, M. 1987. Physical demands of work and health complaints among women working late in pregnancy. Ergonomics 30:689–701. Chesley, L.C. 1976. Blood pressure, edema and proteinuria in pregnancy. Prog. Clin. Biol. Res. 7:19–66. Clapp, J.F., and S. Dickstein. 1984. Endurance exercise and pregnancy outcome. Med. Sci. Sport 16:556–562. Collings, C.A., L.B. Curet, and J.P. Mullin. 1983. Maternal and fetal responses to a maternal aerobic exercise program. Am. J. Obstet. Gynecol. 145:702–707. Creasy, R.K., B.A. Gummer, and G.C. Liggins. 1980. System for predicting spontaneous preterm birth. Obstet. Gynecol. 55:692–695. Dale, E., K.M. Mullinax, and D.H. Bryan. 1982. Exercise during pregnancy: Effects on the fetus. Can. J. Appl. Sport Sci. 7:98–103. Davies, A.M., and W. Dunlop. 1983. Hypertension in pregnancy. Pp. 167–208 in S.L. Barron and A.M. Thomson, eds. Obstetrical Epidemiology. Academic Press, London. Delgado, H., R. Martorell, E. Brineman, and R.E. Klein. 1982. Nutrition and length of gestation. Nutr. Res. 2:117–126. Demakis, J.G., and S.H. Rahimtoola. 1971. Peripartum cardiomyopathy. Circulation 44:964–968. Edwards, M.J. 1986. Hyperthermia as a teratogen: A review of experimental studies and their clinical significance. Teratogenesis Carcinog. Mutagen 6(6):563–582. Erkkola, R. 1976. The physical work capacity of the expectant mother and its effect on pregnancy, labor and the newborn. Int. J. Gynaecol. Obstet. 14:153–159. Estryn, M., M. Kaminski, M. Franc, S. Fernand, and F. Gerstle. 1978. Grossesse et conditions de travail en milieu hospitalier. Rev. Gynecol. Obstet. 73:625–631. Fox, M.E., R.E. Harris, and A.L. Brekken. 1977. The active-duty military pregnancy: A new high-risk category. Am. J. Obstet. Gynecol. 129:705–707. Frame, S., J. Moore, A. Peters, and D. Hall. 1985. Maternal height and shoe size as predictors of pelvic disproportion: An assessment. Br. J. Obstet. Gynecol. 92:1239–1245. Fraser, F.C., and J. Skelton. 1978. Possible teratogenicity of maternal fever (letter). Lancet 2(8090):634. Frisancho, A.R., J. Matos, and L.A. Bollettino. 1984. Influence of growth status and placental function on birth weight of infants born to young still-growing teenagers. Am. J. Clin. Nutr. 40:801–807. Gilstrap, L.C., J.C. Hauth, G.D.V. Hankins, and A. Beck. 1987. Twins: Prophylactic hospitalization and ward rest at early gestational age. Obstet. Gynecol. 69:579–581. Goujon, H., E. Papiernik, and D. Maine. 1984. The prevention of preterm delivery through prenatal care: An intervention study in Martinique. Int. J. Gynaecol. Obstet. 22:339–343. Grunebaum, A., H. Minkoff, and D. Blake. 1987. Pregnancy among obstetricians: A comparison of births before, during and after residency. Am. J. Obstet Gynecol. 157(1):79–83. Habicht J.P., C. Yarbrough, A. Lechtig, and R. E. Klein. 1974. Relation of maternal supplementary feeding during pregnancy to birth weight and other sociobiological factors. Pp. 127–145 in M. Winick, ed. Current Concepts in Nutrition, Vol. 1. Nutrition and Fetal Development. John Wiley, New York. Halperin, L.R., and R.S. Wilroy, Jr. 1978. Maternal hyperthermia and neural tube defects (letter). Lancet 2(8082):212–213. Hediger, M.L., T.O. Scholl, D.H. Belsky, I.G. Ances, and R.W. Salmon. 1989. Patterns of weight gain in adolescent pregnancy: Effects on birthweight and preterm delivery. Obstet. Gynecol. 74(1):6–12.

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Nutrition Issues in Developing Countries: Part I: Diarrheal Diseases - Part II: Diet and Activity During Pregnancy and Lactation Herrera, M.G., J.O. Mora, B. de Paredes, and M. Wagner. 1980. Maternal weight/height and the effect of food supplementation during pregnancy and lactation. Pp. 252–263 in H. Aebi and R. Whitehead, eds. Maternal Nutrition During Pregnancy and Lactation. Hans Huber Publishers, Bern. Herron, M.A., M. Katz, and R.K. Creasy. 1982. Evaluation of a preterm birth prevention program: A preliminary report. Obstet. Gynecol. 59:452–456. Hingson, R.J., J. Alpert, N. Day, E. Dooling, H. Kayne, S. Morelock, E. Oppenheimer, and B. Zuckerman. 1982. Effects of maternal drinking and marijuana use on fetal growth and development. Pediatr. 70:539–546. Homans, D.C. 1985. Peripartum cardiomyopathy. N. Engl. J. Med. 312:1432–1437. Homer, C.J., S.A.A. Beresford, S. James, E. Siegel, and S. Wilcox. 1990a. Work-related physical exertion and risk of preterm, low birthweight delivery. Paediatr. Perinat. Epidemiol. 4(2):161–174. Homer, C.J., S. James, and E. Siegel. 1990b. Work-related psycosocial stress and risk of preterm, low birthweight delivery. Am. J. Public Health 80(2):173–177. Hughes, A.B., A. Jenkins, R.G. Newcomb, and J.F. Pearson. 1987. Symphysis-fundus height, maternal height, labor pattern, and mode of delivery. Am. J. Obstet. Gynecol. 156:644–648. Hytten, F.E., and G.V. Chamberlain. 1980. Clinical Physiology in Obstetrics . Blackwell Scientific Publications, Oxford. Jarrett, J.C., and W.N. Spellacy. 1983. Jogging during pregnancy. An improved outcome. Obstet. Gynecol. 61:705–709. Kaminski, M., and E. Papiernik. 1974. Multifactorial study of the risk of prematurity at 32 weeks of gestation. II. A comparison between an empirical prediction and a discriminant analysis. J. Perinat. Med. 2:37–44. Kaminski, M., J. Goujard, and C. Rumeau-Rouquette. 1973. Prediction of low birthweight and prematurity by a multiple regression analysis with maternal characteristics known since the beginning of the pregnancy. Int. J. Epidemiol. 2:195–204. Kline, J., Z.A. Stein, M.W. Susser, and D. Warburton. 1985. Fever during pregnancy and spontaneous abortion. Am. J. Epidemiol. 121:327–342. Koff, A.K., and E.L. Potter. 1939. The complications associated with excessive development of the human fetus. Am. J. Obstet. Gynecol. 38:412–423. Kramer, M. S. 1987. Determinants of low birth weight: A methodologic assessment and synthesis. Bull. W.H.O. 65:663–667. Kramer, M.S., and C. Sasportas. 1985. Determinants of Intrauterine Growth and Gestational Duration: A Critical Bibliography, 1970–1984. Document NUT/85.10. WHO, Geneva. Kramer, M.S., F.H. McLean, M.E. Boyd, and R.H. Usher. 1988. The validity of gestational age estimation by menstrual dating in term, preterm, and postterm gestations. J. Am. Med. Assoc. 260:3306–3308. Kulpa, P.J., B.M. White, and R. Visscher. 1987. Aerobic exercise in pregnancy. Am. J. Obstet. Gynecol. 156:1395–1403. Langhoff-Roos, J. G. Lindmark, E. Kylberg, and M. Gebre-Medhin. 1987. Energy intake and physical activity during pregnancy in relation to maternal fat accretion and infant birthweight. Br. J. Obstet. Gynecol. 94(12):1178–1185. Lechtig, A., J.P. Habicht, H. Delgado, R.E. Klein, C. Yarbrough, and R. Martorell. 1975. Effect of food supplementation during pregnancy on birthweight. Pediatr. 56:508–520. Leck, I. 1978. Maternal hyperthermia and anencephaly (letter). Lancet 1(8065):671–672. Mamelle, N., and F. Munoz. 1987. Occupational working conditions and preterm birth: A reliable scoring system. Am. J. Epidemiol. 126:150–152. Mamelle, N., B. Laumon, and P. Lazar. 1984. Prematurity and occupational activity during pregnancy. Am. J. Epidemiol. 119:309–322.

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Nutrition Issues in Developing Countries: Part I: Diarrheal Diseases - Part II: Diet and Activity During Pregnancy and Lactation Mamelle, N., I. Bertucat, and F. Munoz. 1989. Pregnant women at work: Rest periods to prevent preterm births? Paediatr. Perinat. Epidemiol. 3:19–28. Manshande, J.P., R. Eeckels, V. Manshande-Desmet, and R. Vlietinck. 1987. Rest versus heavy work during the last weeks of pregnancy: Influence on fetal growth. Br. J. Obstet. Gynecol. 94(11):1059–1067. Marbury, M.C., S. Linn, R.R. Monson, D.H. Wegman, S.C. Schoenbaum, P.G. Stubblefield, and K.J. Ryan. 1984. Work and pregnancy. J. Occup. Med. 26:415–421. Marcoux, S., J. Brisson, and J. Fabia. 1989. The effect of leisure time physical activity on the risk of pre-eclampsia and gestational hypertension. J. Epidemiol. Comm. Health 43(2):147–152. McDonald, E.C., E. Pollitt, W. Mueller, A.M. Hsueh, and R. Sherwin. 1981. The Bacon Chow Study: Maternal nutrition and supplementation and birth weight of offspring. Am. J. Clin. Nutr. 34:2133–2144. Miller, H.C., and T.A. Merritt. 1979. Fetal Growth in Humans. Year Book Medical, Chicago. Mitchell, M.C., and E. Lerner. 1989. Weight gain and pregnancy outcome in underweight and normal weight women. J. Am. Diet. Assoc. 89:634–638. Modanlou, H.D., W.L. Dorchester, A. Thorosian, and R.K. Freeman. 1980. Macrosomia-maternal, fetal, and neonatal implications. Obstet. Gynecol. 55:420–424. Mora, J.O., B. de Paredes, M. Wagner, L. de Navarro, J. Suescun, N. Christiansen, and M.G. Herrera. 1979. Nutritional supplementation and the outcome of pregnancy. I. Birth weight. Am. J. Clin. Nutr. 32:455–462. Murphy, J.F., M. Dauncey, R. Newcombe, J. Garcia, and D. Elbourne. 1984. Employment in pregnancy: Prevalence, maternal characteristics, perinatal outcome. Lancet 1(8387):1163–1166. Naeye, R.L. 1981a. Maternal blood pressure and fetal growth. Am. J. Obstet. Gynecol. 141:780–787. Naeye, R.L. 1981b. Maternal nutrition and pregnancy outcome. Pp. 89–102 in J. Dobbing, ed. Maternal Nutrition in Pregnancy: Eating for Two? Academic Press, London. Naeye, R.L., and E.C. Peters. 1982. Working during pregnancy. Effects on the fetus. Pediatr. 69:724–727. NCHS (National Center for Health Statistics). 1987. Vital Statistics of the United States, 1983. Volume 2. Mortality, Part A. Government Printing Office , Washington, D.C. NRC (National Research Council). 1970. Maternal Nutrition and the Course of Pregnancy. Report of the Committee on Maternal Nutrition, Food and Nutrition Board. National Academy of Sciences, Washington, D.C. 241 pp. Nurminen, T., and K. Kurppa. 1998. Office employment, work with video display terminal, and course of pregnancy: Reference mothers' experience from a Finnish case-referent study of birth defects. Scand. J. Work Environ. Health 14:293–298. Papiernik, E., and M. Kaminski. 1974. Multifactorial study of the risk of prematurity at 32 weeks of gestation. I. A study of the frequency of 30 predictive characteristics. J. Perinat. Med. 2:30–36. Papiernik, E., and M. Vial. 1979. Problèmes actuels de la prévention de la prématurité. Méd. Hyg. 37:108–1665. Papiernik, E., J. Bouyer, J. Dreyfus, D. Collin, G. Winisdorffer, S. Guegen, M. Lecomte, and P. Lazar. 1985. Prevention of preterm births: A perinatal study in Haguenau, France. Pediatr. 76:154–158. Pascoe, J.M., J. Chessare, T. Baugh, L. Urich, and N. Dalongo. 1987. Help with prenatal household tasks and newborn birth weight: Is there an association? J. Dev. Behav. Pediatr. 8:207–212. Pebley, A.R., S.L. Huffman, A.K.M.A. Chowdhury, and P.W. Stupp. 1985. Intrauterine mortality and maternal nutritional status in rural Bangladesh. Popul. Stud. 39:425–440.

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Nutrition Issues in Developing Countries: Part I: Diarrheal Diseases - Part II: Diet and Activity During Pregnancy and Lactation Picone, T.A., L.H. Allen, P.N. Olsen, and M.E. Ferris. 1982. Pregnancy outcome in North American women. II. Effects of diet, cigarette smoking, stress, and weight gain on placentas, and on neonatal physical and behavioral characteristics. Am. J. Clin. Nutr. 36:1214–1224. Pomerance, J.J., L. Gluck, and V.A. Lynch. 1974. Physical fitness in pregnancy: its effect on pregnancy outcome. Am. J. Obstet. Gynecol. 119:867–876. Prentice, A.M. 1980. Variations in maternal dietary intake, birthweight, and breast-milk output in the Gambia. Pp. 167–182 in H. Aebi and R. Whitehead, eds. Maternal Nutrition During Pregnancy and Lactation. Hans Huber Publishers, Bern. Prentice, A.M., R.G. Whitehead, S.B. Roberts, and A.A. Paul. 1981. Long-term energy balance in child-bearing Gambian women. Am. J. Clin. Nutr. 34:2790–2799. Prentice, A.M., R.G. Whitehead, M. Watkinson, W.H. Lamb, and T.J. Cole. 1983. Prenatal dietary supplementation of African women and birth-weight. Lancet 1(8323):489–492. Ribeiro, M.D., Z. Stein, M. Susser, P. Cohen, and R. Neugug. 1982. Prenatal starvation and maternal blood pressure near delivery. Am. J. Clin. Nutr. 35:535–541. Rush, D., H. Davis, and M. Susser. 1972. Antecedents of low birthweight in Harlem, New York City. Int. J. Epidemiol. 1:375–387. Rush, D., Z. Stein, and M. Susser. 1980. A randomized controlled trial of prenatal nutritional supplementation in New York City. Pediatr. 125:567–575. Rush, D., J.M. Alvin, O.A. Kenny, S.S. Johnson, and D.G. Horwitz. 1988a. The National WIC Evaluation: Evaluation of the Special Supplemental Food Program for Women, Infants, and Children. III. Historical study. Am. J. Clin. Nutr. 48:412–428. Rush, D., N.L. Sloan, J. Leighton, J.M. Alvir, D.G. Horvitz, W.B. Seaver, G.C. Garbowski, S.S. Johnson, R.A. Kulka, M. Holt, J.W. Devote, J.T. Lynch, M. Beebe Woodside, and D.S. Shanklin. 1988b. The National WIC Evaluation: Evaluation of the Special Supplemental Food Program for Women, Infants, and Children. V. Longitudinal study of pregnant women. Am. J. Clin. Nutr. 48:439–483. Rydhstrom, H. 1988. Twin pregnancy and the effects of prophylactic leave of absence on pregnancy duration and birth weight. Acta Obstet. Gynecol. Scand. 67(1):81–84. Sachs, B.P., D.A.J. Brown, S.G. Driscoll, E. Schulman, D. Ackin, B.J. Ransil, and J.T. Jewett. 1987. Maternal mortality in Massachusetts: Trends and prevention. N. Engl. J. Med. 316:667–672. Saunders, M.C., J.S. Dick, I.M. Brown, K. McPherson, and I. Chalmers. 1985. The effects of hospital admission for bed rest on the duration of twin pregnancy: A randomized trial. Lancet 2(8459):793–795. Saurel-Cubizolles, M.J., and M. Kaminski. 1983. Pregnant women at work. Lancet 1(8322):475. Saurel-Cubizolles, M.J., and M. Kaminski. 1987. Pregnant women's working conditions and their changes during pregnancy: A national study in France. Br. J. Ind. Med. 44:236–243. Saurel-Cubizolles, M.J., M. Kaminski, and C. Rumeau-Rouquette. 1982. Activité professionelle des femmes enceintes, surveillance prénatale et issue de la grossesse. J. Gyn. Obstét. Biol. Réprod. 11:959–967. Saurel-Cubizolles, M.J., M. Kaminski, J. Llado-Arkhipoff, C. du Mazaubrun, M. Estryn-Behar, C. Berthier, M. Mouchet, and C. Kelfa. 1985. Pregnancy and its outcome among hospital personnel according to occupation and working conditions. J. Epidemiol. Comm. Health 39:129–134. Schneider, K.T.M., A. Hoch, and R. Hoch. 1985. Premature contractions: Are they caused by maternal standing? Acta Genet. Med. Germellol. 34:175–178. Shepard, M.J., K.G. Hellenbrand, and M.B. Bracken. 1986. Proportional weight gain and complications of pregnancy, labor and delivery in healthy women of normal prepregnancy stature. Am. J. Obstet. Gynecol. 155:947–954.

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Nutrition Issues in Developing Countries: Part I: Diarrheal Diseases - Part II: Diet and Activity During Pregnancy and Lactation Shilling, S., and N.R. Lalich. 1984. Maternal occupation and industry and the pregnancy outcome of U.S. married women. Public Health Rep. 99:152–161. Shiota, K. 1982. Neural tube defects and maternal hyperthermia in early pregnancy. Epidemiology in a human embryo population. Am. J. Med. Genet. 12:281–288. Silverman, J., J. Kline, M. Hutzler, Z.A. Stein, and D. Warburton. 1985. Maternal employment and the chromosomal characteristics of spontaneously aborted conception. J. Occup. Med. 27:427–438. Smith, D.W., S.K. Clarren, and M.A.S. Harvey. 1978. Hyperthermia as a positive teratogenic agent. J. Pediatr. 92:878–883. Stein, Z., M. Susser, G. Saenger, and F. Marolla. 1975. Famine and Human Development: The Dutch Hunger Winter of 1944–1945. Oxford University, New York. Stengel, B., M.J. Saurel-Cubizolles, and M. Kaminski. 1986. Pregnant immigrant women: Occupational activity, antenatal care and outcome. Int. J. Epidemiol. 15:533–539. Stengel, B., M.J. Saurel-Cubizolles, and M. Kaminski. 1987. Healthy worker effect and pregnancy: Role of adverse obstetric history and social characteristics. J. Epidemiol. Comm. Health 41:312–320. Tafari, N., R.L. Naeye, and A. Gobezie. 1980. Effects of maternal undernutrition and heavy physical work during pregnancy on birth weight. Br. J. Obstet. Gynaecol. 87:222–226. Thomson, A.M., and W.Z. Billewicz. 1957. Clinical significance of weight trends during pregnancy. Br. Med. J. 1:243–247. Tompkins, W., D. Wiehl, and R. Mitchell. 1955. The underweight patient as an increased obstetric hazard. Am. J. Obstet. Gynecol. 69:114–123. Ulrich, M. 1982. Fetal growth patterns in a population of Danish newborn infants. Acta Paediatr. Scand. 292:5–45. Varma, T.R. 1984. Maternal weight and weight gain in pregnancy and obstetric outcome. Int. J. Gynecol. Obstet. 22:161–166. Viegas, O.A.C., P.H. Scott, T.J. Cole, P. Eaton, P.G. Needham, and B.A. Wharton. 1982. Dietary protein energy supplementation of pregnant Asian mothers at Sorrento, Birmingham. II. Selective during third trimester only. Br. Med. J. 285:592–595. Villar, J., M.J. Khourz, F.F. Finucane and H.L. Delgado. 1986. Differences in the epidemiology of prematurity and intrauterine growth retardation. Early Hum. Dev. 14:307–320. Warkany, J. 1986. Teratogen update: Hyperthermia. Teratology 33:365–371. Whitehead, R.G., M.G.M. Rowland, M. Hutton, A.M. Prentice, E. Muller, and A. Paul. 1978. Factors influencing lactation performance in rural Gambian mothers. Lancet 2(8082):178–181. Williams, J.H. 1984. Employment in pregnancy (letter). Lancet 2(8394):103–104. Winikoff, B., and C.H. Debrovner. 1981. Anthropometric determinants of birth weight. Obstet. Gynecol. 58:678–684. Wong, S.C., and D.C. McKenzie. 1987. Cardiorespiratory fitness during pregnancy and its effect on outcome. Int. J. Sports Med. 8:79–83. WHO (World Health Organization). 1965a. Expert Committee on Eclampsia. Special Technical Report No. 302. WHO, Geneva. WHO (World Health Organization). 1965s. Nutrition in Pregnancy and Lactation. Report of a WHO Expert Committee. Technical Report Series No. 302. World Health Organization, Geneva. WHO (World Health Organization). 1985. Report of Interregional Meeting on Maternal Mortality, November 11–15. WHO, Geneva. Zuckerman, B.S., D.A. Frank, R. Hingson, S. Morelock, and H.L. Kayne. 1986. Impact of maternal work outside the home during pregnancy on neonatal outcome. Pediatr. 77:459–464.

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